Contribution of laminar myofiber architecture to load-dependent changes in mechanics of LV myocardium

Abstract

Takayama, Yasuo, Kevin D. Costa, and James W. Covell. Contribution of laminar myofiber architecture to load-dependent changes in mechanics of LV myocardium. Am J Physiol Heart Circ Physiol 282: H1510-H1520, 2002; 10.1152/ajpheart.00261.2001.-The ventricular myocardium consists of a syncytium of myocytes organized into branching, transmurally oriented laminar sheets approximately four cells thick. When systolic deformation is expressed in an axis system determined by the anatomy of the laminar architecture, laminar sheets of myocytes shear and laterally extend in an approximately radial direction. These deformations account for ϳ90% of normal systolic wall thickening in the left ventricular free wall. In the present study, we investigated whether the changes in systolic and diastolic function of the sheets were sensitive to alterations in systolic and diastolic load. Our results indicate that there is substantial reorientation of the laminar architecture during systole and diastole. Moreover, this reorientation is both site and load dependent. Thus as end-diastolic pressure is increased and the left ventricular wall thins, sheets shorten and rotate away from the radial direction due to transverse shearing, opposite of what occurs in systole. Both mechanisms of thickening contribute substantially to normal left ventricular wall function. Whereas the relative contributions of shear and extension are comparable at the base, sheet shear is the predominant factor at the apex. The magnitude of shortening/extension and shear increases with preload and decreases with afterload. These findings underscore the essential contribution of the laminar myocardial architecture for normal ventricular function throughout the cardiac cycle. myocardium; wall thickening; systole; diastole THE VENTRICULAR MYOCARDIUM consists of a syncytium of myocytes organized into branching transmurally oriented laminar sheets approximately four cells thick (14). Recent evidence indicates that this laminar structure contributes importantly to systolic function. When systolic deformation is expressed in an axis system determined by the anatomy of the laminar architecture, laminar sheets of myocytes shear and laterally extend in an approximately radial direction. These deformations account for ϳ90% of normal systolic wall thickening in the left ventricular (LV) free wall. In a recent study (5) from this laboratory, we found regional variations in the relative contribution of sheet extension and shear to wall thickening. In the free wall of the ventricle, sheet extension accounted for the majority of wall thickening, whereas in the septum, sheet shear was the predominant factor. Systolic wall thickening is a commonly employed index of regional myocardial performance (8) in both clinical and experimental studies. However, wall thickening varies both transmurally and regionally (7). These variations were reported in clinical studies (3) using magnetic resonance imaging (MRI). Moreover, Villarreal et al. (36) have shown regional variations in the sensit...

Direct measurement of transmural laminar architecture in the anterolateral wall of the ovine left ventricle: new implications for wall thickening mechanics

“…This transmural myofiber distribution has been described in many species, including humans (12), using histology (14,18,23,28) or diffusion tensor magnetic resonance imaging (4,10,25). This helical myofiber orientation is relatively preserved among different species, ranging from approximately −60° to +60° from epicardium to endocardium, with circumferential fibers at midwall, although some studies have shown some variation from apex to base (6,23,24). The present study is the first to report transmural distribution of α in the ovine heart, but our data are consistent with these previously published reports from other species.…”

“…The helical arrangement of the fibers may account for some of this disparity (20), but an additional important mechanism appears to be sheet deformation (19,22). Laminar shear, extension, and thinning or thickening are thought to contribute to wall thickness changes (6,7,24).Fiber orientation, which can be measured directly, has been found in several species to vary from approximately −60° at the epicardium to +60° at the endocardium (4,10,12,14,23,28). Until recently, however, sheet orientation could only be inferred indirectly from the directions of fiber and cleavage planes from three orthogonal views (6).…”

“…Therefore, previous studies have measured cleavage plane angles in two orthogonal planes tangent to the cardiac coordinates (X 2-3 and X 1-3 ) and α in the X 1-2 plane, and these cleavage plane angles were mathematically transformed to correspond to those in the plane in which the X s axis (X cf-3 ) lies (1,6,17,24). Therefore, indirect β measurements using such mathematical transformations must assume a continuous distribution of a predominant sheet family from the measurement plane (X 2 ,X 3 or X 1 ,X 3 ) to the extrapolated (X cf ,X 3 ) plane.Previous indirect measurements in canine hearts, mostly from the anterior wall, have shown a consistently negative β (approximately −30° to −40°) through the wall depth, (2,5,6,17,24) or a progression from negative to positive β or vice versa (within −90° and +90°) across the heart wall (6,15,16). These transmural patterns also vary substantially from apex to base (6,16,24) and in different regions of the LV (16,17).…”

“…The results of the present study encourage a thorough and systematic study of the entire LV, but this is beyond the scope of the present study. Variation in sheet distribution has been shown from apex to base (6,16,24), and it is possible that there is variation among different species as well. The site and species variation may account for the differences in the magnitudes and signs of β reported from previous experiments, which have largely focused on the basal and apical anterior LV walls of canine hearts.…”

Left Ventricular Form and Function Revisited: Applied Translational Science to Cardiovascular Ultrasound Imaging

“…These studies established that fiber orientation was a function of transmural location, with fiber direction being predominantly longitudinal in the endocardial region; transitioning into a circumferential direction in the midwall and becoming longitudinal again over the epicardial surface. Myofiber morphology was described either based on orientation of individual fibers or as multiple myocyte 'sheet' arrangements separated by extensive 'sheet cleavage' planes (17)(18)(19)(20). Some investigators depicted the LV as a complex nested continuum where the myofibers entwined to form a mechanical and electrical syncytium (21,22).…”