Role of tissue structure on ventricular wall mechanics

Abstract

It is well known that systolic wall thickening in the inner half of the left ventricular (LV) wall is of greater magnitude than predicted by myofiber contraction alone. Previous studies have related the deformation of the LV wall to the orientation of the laminar architecture. Using this method, wall thickening can be interpreted as the sum of contributions due to extension, thickening, and shearing of the laminar sheets. We hypothesized that the thickening mechanics of the ventricular wall are determined by the structural organization of the underlying tissue, and may not be influenced by factors such as loading and activation sequence. To test this hypothesis, we calculated finite strains from biplane cineradiography of transmural markers implanted in apical (n = 22) and basal (n = 12) regions of the canine anterior LV free wall. Strains were referred to three-dimensional laminar microstructural axes measured by histology. The results indicate that sheet angle is of opposite sign in the apical and basal regions, but absolute value differs only in the subepicardium. During systole, shearing and extension of the laminae contribute the most to wall thickening, accounting for >90% (transmural average) at both apex and base. These two types of deformation are also most prominent during diastolic inflation. Increasing afterload has no effect on the pattern of systolic wall thickening, nor does reversing transmural activation sequence. The pattern of wall thickening appears to be a function of the orientation of the laminar sheets, which vary regionally and transmurally. Thus, acute interventions do not appear to alter the contributions of the laminae to wall thickening, providing further evidence that the structural architecture of the ventricular wall is the dominant factor for its regional mechanical function.

Fig. 1

A: schematic representation of the left ventricle with bead arrays at the apex and base (1/3 and 2/3 of the distance from apex and base, respectively). X₁, circumferential axis; X₂, longitudinal axis; X₃, radial axis; LAD, left anterior descending; LCX, left circumflex. B: schematic representation of local fiber-sheet axes. Fiber angle (α) was measured in the X₁-X₂ plane at each wall depth with reference to positive X₁. Sheet angle (β) was measured in the plane perpendicular to the fiber angle at each wall depth with reference to positive X₃. X_f, fiber axis, X_s, sheet axis, X_n, axis oriented normal to the sheet plane.

Fig. 2

Contributions of different types of sheet deformation to wall thickening. Schematics show how a portion of the wall can thicken from an undeformed (top) to deformed (bottom) state, based on sheet movement. A: extension of the sheets, B: thickening of the sheets, C: shearing between sheets. Wall thickening is indicated by the widening of the vertical bars, i.e. an increase in the radial direction, r. Open circles represent myofibers, gray bars represent sheets. s, sheet direction; n, sheet normal direction.

Fig. 3

Sheet angles. Angle = 0° indicates a radial orientation. Sheet angle has opposite sign at apical and basal sites, but similar absolute values. The largest angle occurred at the midwall of each site. There was a significant transmural gradient at each site (RMANOVA, p<0.05). * p < 0.05 vs other depths. At each depth, the base was significantly different from the apex. † p < 0.05 vs. same depth, by unpaired t-test.

Fig. 4

End-systolic contributions to wall thickening. Contributions to wall thickening due to sheet extension (A), sheet thickening (B), and sheet shearing (C). Relative contributions of sheet deformation to wall thickening were similar at both sites. There were significant transmural gradients due to sheet extension and sheet shearing at the basal site (RMANOVA, p<0.05). * p < 0.05 vs other depths. At the sub-epicardium only, the relative contributions to wall thickening were significantly different between the apical and basal sites († p < 0.05 vs. same depth, by unpaired t-test).

Fig. 5

Contributions of sheet deformation to wall thinning during diastolic loading. Bars show relative contributions during diastolic inflation from a reference configuration of 3 mmHg to a deformed configuration of 8 mmHg (“Low”), 13 mmHg (“Medium”), or 18 mmHg (“High”). Contributions due to sheet shortening, thinning, and shearing were similar at apex (A) and base (B), and their transmural gradients were not significantly affected by diastolic load (* p < 0.05 vs. other depths).

Fig. 6

Effect of afterload on wall thickening. Bars indicate relative contributions to wall thickening at midwall and sub-endocardial depths. Increased afterload was achieved by administering methoxamine (“Methox.”). There were no significant differences at the apex (A) or base (B) in any of the contributers. Sub-epicardial values were excluded due to insufficient strain magnitude to perform calculation.

Fig. 7

Time course of wall thickening during pacing during atrial pacing (A), local endocardial pacing (B), or local epicardial pacing (C). Bar height indicates magnitude of radial strain at 50% depth as a function of time for one cardiac cycle, in a representative animal. Stacked bars distinguish the relative contributions of the different sheet motions. Though the time courses are different, the contributions of sheet deformation to wall thickening are relatively constant throughout the cycle as well as with different pacing modes. Differences tended to be greatest during the isovolumic phases.

Fig. 8

Average contributions to wall thickening during pacing. Stacked bars represent the average of each of the components of wall thickening at three transmural depths. For all components, there was a significant transmural gradient; however, ventricular pacing (endocardial or epicardial) was not significantly different from atrial pacing, nor was there a significant interaction with depth (2-way RMANOVA).