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. 2005 Mar;288(3):H1324-30.
doi: 10.1152/ajpheart.00813.2004. Epub 2004 Nov 18.

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

Katherine B Harrington  1 , Filiberto Rodriguez, Allen Cheng, Frank Langer, Hiroshi Ashikaga, George T Daughters, John C Criscione, Neil B Ingels, D Craig Miller
Affiliations

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

Katherine B Harrington et al. Am J Physiol Heart Circ Physiol. 2005 Mar.

Abstract

Laminar, or sheet, architecture of the left ventricle (LV) is a structural basis for normal systolic and diastolic LV dynamics, but transmural sheet orientations remain incompletely characterized. We directly measured the transmural distribution of sheet angles in the ovine anterolateral LV wall. Ten Dorsett-hybrid sheep hearts were perfusion fixed in situ with 5% buffered glutaraldehyde at end diastole and stored in 10% formalin. Transmural blocks of myocardial tissue were excised, with the edges cut parallel to local circumferential, longitudinal, and radial axes, and sliced into 1-mm-thick sections parallel to the epicardial tangent plane from epicardium to endocardium. Mean fiber directions were determined in each section from five measurements of fiber angles. Each section was then cut transverse to the fiber direction, and five sheet angles (beta) were measured and averaged. Mean fiber angles progressed nearly linearly from -41 degrees (SD 11) at the epicardium to +42 degrees (SD 16) at the endocardium. Two families of sheets were identified at approximately +45 degrees (beta(+)) and -45 degrees (beta(-)). In the lateral region (n = 5), near the epicardium, sheets belonged to the beta(+) family; in the midwall, to the beta(-) family; and near the endocardium, to the beta(+) family. This pattern was reversed in the basal anterior region (n = 4). Sheets were uniformly beta(-) over the anterior papillary muscle (n = 2). These direct measurements of sheet angles reveal, for the first time, alternating transmural families of predominant sheet angles. This may have important implications in understanding wall mechanics in the normal and the failing heart.

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Figures

Fig. 1
Fig. 1
Coordinate systems. A: transmural fiber angle (α) and sheet angle (β) were determined in the midlateral free wall of the left ventricle (LV), between the papillary muscles. Local “cardiac coordinates” (X1, X2, and X3, representing a Cartesian coordinate system) are shown. APM, anterolateral papillary muscle; PPM, posteromedial papillary muscle. B: a transmural tissue block was excised from each heart, with the edges of the block cut parallel to the local circumferential (X1), longitudinal (X2), and radial (X3) axes at the midlateral LV wall; α was measured from serial sections cut parallel to the X1-X2 plane at different transmural depths. C: at a given transmural depth, measured α and β are used to define local “fiber-sheet” coordinates with basis vectors of fiber (Xf) axis, sheet axis perpendicular to Xf within sheet plane (Xs), and axis normal to the sheet plane (Xn). Xf, Xs, and Xn represent a Cartesian coordinate system. Xf lies in the X1-X2 plane; Xs lies in the plane defined by X3 and the axis normal to the fiber direction (Xcf), which is not shown.
Fig. 2
Fig. 2
Measurement of α and β. A: each transmural slice from the block of tissue was affixed to a note card with positive X1 pointing to the right, positive X2 pointing up, and positive X3 pointing away from the paper. Positive X1 represented α = 0°, with a negative α (as shown) defined as a clockwise rotation about X1. Two parallel cuts separated by ~1 mm were made normal to Xf axis in each section along the Xcf axis. Xf, Xcf, and X3 present another Cartesian coordinate system. B: resulting slices were rotated 90° about Xcf, so that Xf pointed out of the page and β lay in the plane of observation, with positive X3 perpendicular to Xcf (defined by the paper attached to the specimen), allowing direct measurement of β corresponding to α at each transmural depth. C: a cryostat was used to cut frozen specimens into 8- to 10-μm-thick sections, which were carefully transferred to a glass slide. During the cutting process, a predominant β was observed from each frozen specimen mounted on the cryostat. Each slice was observed and photographed at low-power (×25) magnification. Values of β were measured along gaps between cleavage planes that first appeared as the specimen dried and corresponded to the predominant angle observed in each frozen specimen, thereby minimizing the likelihood of measuring dehydration artifact. Positive X3 was perpendicular to Xcf and represented β = 0°; a counterclockwise rotation was represented by a negative β.
Fig. 3
Fig. 3
A: transmural distribution of α in the lateral wall for all 5 animals. B: transmural distribution of β in the lateral wall for all 5 animals. Values of β were centered around two “families”: one at approximately +45° and one at approximately −45°. Near the epicardium, β belonged to the +45° family, in the midwall to the −45° family, and near the endocardium to the +45° family. Epi, epicardium; Endo, endocardium.
Fig. 4
Fig. 4
Representative images obtained using the direct histological method. Left: a specimen with β values that fall into the β+ family. Right: a specimen with β values that fall into the β− family.
Fig. 5
Fig. 5
Conceptual model synthesizing data from anterior, anterolateral, and lateral equatorial regions of the heart. Left: representation of the sheets at 20, 50, and 80% wall depth from the epicardium. Black lines on the surface of the sheets correspond qualitatively to measured α, with negative α values near the epicardium, circumferential α values (0°) at midwall, and positive α values near the epicardium. Left regions represent data from the anterior wall, with sheets belonging to the β− family at 20%, to the β+ family at 50%, and to the β− family at 80% wall depth. Middle regions represent the region over the anterior papillary muscle, with sheets belonging to the β− family throughout the wall. Right regions represent data from the lateral region, with sheets belonging to the β+ family at 20%, to the β− family at 50%, and to the β+ family at 80% wall depth from the epicardium.
Fig. 6
Fig. 6
Two-dimensional representation of the plane, which in reality twists through the wall, as the sheets are perpendicular to the helically progressing fibers across the wall. Solid and dashed lines, lateral myolaminar sheets in systole and diastole, respectively. With alternating sheet families through the wall, wall thickening (D) may be due to laminar transverse shear (A), laminar extension (B), and laminar thinning (C) of each population.
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