Transmural myocardial mechanics during isovolumic contraction

Abstract

Objectives: We sought to resolve the 3-dimensional transmural heterogeneity in myocardial mechanics observed during the isovolumic contraction (IC) phase.

Background: Although myocardial deformation during IC is expected to be little, recent tissue Doppler imaging studies suggest dynamic myocardial motions during this phase with biphasic longitudinal tissue velocities in left ventricular (LV) long-axis views. A unifying understanding of myocardial mechanics that would account for these dynamic aspects of IC is lacking.

Methods: We determined the time course of 3-dimensional finite strains in the anterior LV of 14 adult mongrel dogs in vivo during IC and ejection with biplane cineradiography of implanted transmural markers. Transmural fiber orientations were histologically measured in the heart tissue postmortem. The strain time course was determined in the subepicardial, midwall, and subendocardial layers referenced to the end-diastolic configuration.

Results: During IC, there was circumferential stretch in the subepicardial layer, whereas circumferential shortening was observed in the midwall and the subendocardial layer. There was significant longitudinal shortening and wall thickening across the wall. Although longitudinal tissue velocity showed a biphasic profile; tissue deformation in the longitudinal as well as other directions was almost linear during IC. Subendocardial fibers shortened, whereas subepicardial fibers lengthened. During ejection, all strain components showed a significant change over time that was greater in magnitude than that of IC. Significant transmural gradient was observed in all normal strains.

Conclusions: IC is a dynamic phase characterized by deformation in circumferential, longitudinal, and radial directions. Tissue mechanics during IC, including fiber shortening, appear uninterrupted by rapid longitudinal motion created by mitral valve closure. This study is the first to report layer-dependent deformation of circumferential strain, which results from layer-dependent deformation of myofibers during IC. Complex myofiber mechanics provide the mechanism of brief clockwise LV rotation (untwisting) and significant wall thickening during IC within the isovolumic constraint.

Figure 1. Study Setup

(A) Experimental setup: The transmural bead set (~10 mm) was implanted between the first (D₁) and the second diagonal branch (D₂) of the left anterior descending (LAD) artery. To provide end points for a left ventricular (LV) long axis, gold beads were sutured to the apical dimple (apex bead) and on the epicardium at the bifurcation of LAD and left circumflex (LCx) (base bead). (B) LV myocardium within the bead set. The LV myocardium consists of myofibers (X_f) that run parallel to the epicardial tangent plane and are arranged in radially oriented laminae or sheets (X_s). The principal fiber orientation presents a gradual counterclockwise rotation from epicardium to endocardium, resulting in a local architecture of myofibers resembling a spiral staircase with a transmural angle gradient spanning ~120°. The laminar or sheet structure of the myocardium consists of a layered arrangement of myofibers. X₁ = circumferential axis; X₂ = longitudinal axis; X₃ = radial axis; X_f = fiber axis; X_s = sheet axis; X_n = axis oriented normal to the sheet plane. (C) Isovolumic contraction (IC) was defined as the period beginning at end diastole (ED) (peak of surface ECG R-wave) and ending at aortic valve opening, which was derived from crossover between LV pressure (LVP) and central aortic pressure (AoP). ECG = electrocardiogram; LAP = left atrial pressure.

Figure 2. Time Course of Finite Strains in Local Cardiac Coordinates

Values are mean (n = 14). E₁₁ = circumferential strain; E₂₂ = longitudinal strain; E₃₃ = radial strain; E₁₂ = circumferential-longitudinal shear strain; E₂₃ = longitudinal-radial shear strain; E₁₃ = circumferential-radial shear strain. Note different scales for normal and shear strains. AVO = aortic valve opening; ED = end diastole; IC = isovolumic contraction.

Figure 3. Time Course of Myocardial Location, Velocity, and Strain in the Longitudinal Direction

Values are mean (n = 14). During IC, the myocardium moves toward the apex (= positive direction), resulting in a monophasic motion. The myocardial velocity initially increases, then decreases and finally increases again, resulting in a biphasic waveform. In contrast to the complex change in location and velocity, longitudinal strain shows a relatively straight change during IC. Longitudinal location and velocity are expressed in arbitrary units. Abbreviations as in Figure 2.

Figure 4. Time Course of Finite Strains in Fiber-Sheet Coordinates

Values are mean (n = 14). Note different scales for normal and shear strains. E_ff = fiber strain; E_ss = sheet strain, E_nn = strain normal to the sheet plane; E_fs = fiber-sheet shear strain; E_sn = sheet shear strain; E_fn = fiber-normal shear strain. Abbreviations as in Figure 2.

Figure 5. Time Course of Fiber and Sheet Angle Change From the End-Diastolic Configuration and Relative Myocardial Volume

Angles are given in degrees (deg), and the myocardial volumes are expressed as volume relative to 1.00 at end diastole. Abbreviations as in Figure 2.

Figure 6. Myocardial Deformation During IC

Significant sheet extension (E_ss) and thinning (E_nn) occur, which contributes to radial wall thickening (E₃₃). Myofibers shorten (E_ff) at the endocardium, which is reflected by circumferential (E₁₁) and longitudinal shortening (E₂₂). In contrast, myofibers stretch (E_ff) at the epicardium, which contributes to circumferential stretch (E₁₁) but the myocardium shortens longitudinally (E₂₂). Abbreviations as in Figure 2.

Figure 7. Mechanism of Brief LV Untwisting During IC

During isovolumic contraction, electrical activation initiated in the endocardial Purkinje fibers shortens endocardial fibers (dashed lines) wrapped in a right-handed helix. Circumferential components of force (arrows) are generated by endocardial fiber shortening, which rotates the LV about the long axis clockwise as viewed from the apex (untwisting). During ejection, electrical activation reaches the epicardium and shortens epicardial fibers (solid lines) wrapped in an opposite, left-handed helix, which rotates the LV counterclockwise (twisting). Twisting force by epicardial shortening overcomes untwisting force by endocardial shortening because the torque of the epicardial force is larger because of a greater radius of the epicardial fiber from the central LV long axis. Figure illustration by Rob Flewell. Modified from Ingels et al. (28). LV = left ventricular; other abbreviations as in Figure 2.

Figure 8. Sheet Angle Change During Isovolumic Contraction and Ejection

Sheet angles are measured with reference to the positive radial axis (X₃). The left panel shows a negative sheet angle at end diastole. During isovolumic contraction, there is a significant negative sheet angle change that would act to decrease wall thickness (center panel). During ejection, in contrast, there is a greater positive sheet angle change (right panel) that overcompensates the negative sheet angle change during IC, which acts to thicken the wall at aortic valve closure.