Myofiber angle distributions in the ovine left ventricle do not conform to computationally optimized predictions

Abstract

Recent computational models of optimized left ventricular (LV) myofiber geometry that minimize the spatial variance in sarcomere length, stress, and ATP consumption have predicted that a midwall myofiber angle of 20 degrees and transmural myofiber angle gradient of 140 degrees from epicardium to endocardium is a functionally optimal LV myofiber geometry. In order to test the extent to which actual fiber angle distributions conform to this prediction, we measured local myofiber angles at an average of nine transmural depths in each of 32 sites (4 short-axis levels, 8 circumferentially distributed blocks in each level) in five normal ovine LVs. We found: (1) a mean midwall myofiber angle of -7 degrees (SD 9), but with spatial heterogeneity (averaging 0 degrees in the posterolateral and anterolateral wall near the papillary muscles, and -9 degrees in all other regions); and (2) an average transmural gradient of 93 degrees (SD 21), but with spatial heterogeneity (averaging a low of 51 degrees in the basal posterior sector and a high of 130 degrees in the mid-equatorial anterolateral sector). We conclude that midwall myofiber angles and transmural myofiber angle gradients in the ovine heart are regionally non-uniform and differ significantly from the predictions of present-day computationally optimized LV myofiber models. Myofiber geometry in the ovine heart may differ from other species, but model assumptions also underlie the discrepancy between experimental and computational results. To test the predictive capability of the current computational model would we propose using an ovine specific LV geometry and comparing the computed myofiber orientations to those we report herein.

Figure 1

Each heart was systematically sectioned for quantitative histologic analysis of the myofiber helix angle. (A) Basal, mid-equatorial (E1 and E2), and apical slices were sliced out of each heart. (B) Each slice was then sectioned into sixteen tissue blocks and eight anatomical sectors (numbered) were used for histologic analysis. Eight chunks of remaining tissue (not numbered) are shown in approximate anatomical location, viewed from base to apex. (C) A “cardiac” coordinate system was defined for each block to enable calculation of the myofiber angle (X₁–circumferential, X₂–longitudinal, X₃–radial). (D) The myofiber angle for each transmural section was measured using computer software and was referenced to the local X₁ axis.

Figure 2

Transmural myofiber angles in each of the 32 anatomical sectors, color-coded for each heart. The cubic fit is shown in each sector as a black line, with 95% confidence intervals in gray. The anterior papillary muscle was located between the anterior and anterior-lateral sectors and the posterior papillary muscle was located between the posterior and posterior-lateral sectors.

Figure 3

Direct comparison of myofiber inclination angles obtained in the ovine left ventricle (white dots) and the simulation results of Vendelin et al (Vendelin, Bovendeerd et al., 2002) plotted in the space of myofiber angle transmural slope (α_slope, degrees) and midwall myofiber angle (α_mid, degrees). Vendelin’s approximate optimal myofiber geometry is shown as a ”v”. Results extracted from Streeter (Streeter, Spotnitz et al., 1969)(“S”), Ashikaga (Ashikaga, Omens et al., 2004)(“A”), Greenbaum (Greenbaum, Ho et al., 1981)(”G”), and Nielsen(Nielsen, Le Grice et al., 1991) (“N”) are also shown. Our results from the ovine left ventricle demonstrate a range of myofiber geometries all of which deviate from the optimal results predicted by Vendelin et al. Measured myofiber geometries in the ovine left ventricle, however, do fall within a relatively narrow range of spatial variance in strain, stress, and ATP consumption.