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Technical Brief

Numerical Evaluation of Myofiber Orientation and Transmural Contractile Strength on Left Ventricular Function

[+] Author and Article Information
Xiaoyan Zhang

Department of Mechanical Engineering,
University of Kentucky,
Lexington, KY 40506;
Center for Computational Sciences,
University of Kentucky,
Lexington, KY 40506

Premi Haynes, Kenneth S. Campbell

Department of Physiology,
University of Kentucky,
Lexington, KY 40506;
Center for Muscle Biology,
University of Kentucky,
Lexington, KY 40506

Jonathan F. Wenk

Department of Mechanical Engineering,
University of Kentucky,
269 Ralph G. Anderson Building,
Lexington, KY 40506;
Department of Surgery,
University of Kentucky,
Lexington, KY 40506
e-mail: wenk@engr.uky.edu

1Corresponding author.

Manuscript received June 24, 2014; final manuscript received October 30, 2014; published online February 5, 2015. Assoc. Editor: Jonathan Vande Geest.

J Biomech Eng 137(4), 044502 (Apr 01, 2015) (6 pages) Paper No: BIO-14-1291; doi: 10.1115/1.4028990 History: Received June 24, 2014; Revised October 30, 2014; Online February 05, 2015

The left ventricle (LV) of the heart is composed of a complex organization of cardiac muscle fibers, which contract to generate force and pump blood into the body. It has been shown that both the orientation and contractile strength of these myofibers vary across the ventricular wall. The hypothesis of the current study is that the transmural distributions of myofiber orientation and contractile strength interdependently impact LV pump function. In order to quantify these interactions a finite element (FE) model of the LV was generated, which incorporated transmural variations. The influences of myofiber orientation and contractile strength on the Starling relationship and the end-systolic (ES) apex twist of the LV were assessed. The results suggest that reductions in contractile strength within a specific transmural layer amplified the effects of altered myofiber orientation in the same layer, causing greater changes in stroke volume (SV). Furthermore, when the epicardial myofibers contracted the strongest, the twist of the LV apex was greatest, regardless of myofiber orientation. These results demonstrate the important role of transmural distribution of myocardial contractile strength and its interplay with myofiber orientation. The coupling between these two physiologic parameters could play a critical role in the progression of heart failure.

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References

Hsu, E. W., Muzikant, A. L., Matulevicius, S. A., Penland, R. C., and Henriquez, C. S., 1998, “Magnetic Resonance Myocardial Fiber-Orientation Mapping With Direct Histological Correlation,” Am. J. Physiol., 274(5), pp. H1627–H1634. [PubMed]
LeGrice, I. J., Smaill, B. H., Chai, L. Z., Edgar, S. G., Gavin, J. B., and Hunter, P. J., 1995, “Laminar Structure of the Heart: Ventricular Myocyte Arrangement and Connective Tissue Architecture in the Dog,” Am. J. Physiol., 269(2), pp. H571–H582. [PubMed]
Streeter, D. D., Jr., Spotnitz, H. M., Patel, D. P., Ross, J., Jr., and Sonnenblick, E. H., 1969, “Fiber Orientation in the Canine Left Ventricle During Diastole and Systole,” Circ. Res., 24(3), pp. 339–347. [CrossRef] [PubMed]
Beladan, C. C., Calin, A., Rosca, M., Ginghina, C., and Popescu, B. A., 2013, “Left Ventricular Twist Dynamics: Principles and Applications,” Heart, 100(9), pp. 731–740. [CrossRef] [PubMed]
Sengupta, P. P., Khandheria, B. K., Korinek, J., Wang, J. W., Jahangir, A., Seward, J. B., and Belohlavek, M., 2006, “Apex-to-Base Dispersion in Regional Timing of Left Ventricular Shortening and Lengthening,” J. Am. Coll. Cardiol., 47(1), pp. 163–172. [CrossRef] [PubMed]
Vendelin, M., Bovendeerd, P. H., Engelbrecht, J., and Arts, T., 2002, “Optimizing Ventricular Fibers: Uniform Strain or Stress, but Not ATP Consumption, Leads to High Efficiency,” Am. J. Physiol.: Heart Circ. Physiol., 283(3), pp. H1072–H1081. [PubMed]
Eriksson, T. S. E., Prassl, A. J., Plank, G., and Holzapfel, G. A., 2013, “Influence of Myocardial Fiber/Sheet Orientations on Left Ventricular Mechanical Contraction,” Math. Mech. Solids, 18(6), pp. 592–606. [CrossRef]
Bovendeerd, P. H., Arts, T., Huyghe, J. M., van Campen, D. H., and Reneman, R. S., 1992, “Dependence of Local Left Ventricular Wall Mechanics on Myocardial Fiber Orientation: A Model Study,” J. Biomech., 25(10), pp. 1129–1140. [CrossRef] [PubMed]
Mullins, P. D., and Bondarenko, V. E., 2013, “A Mathematical Model of the Mouse Ventricular Myocyte Contraction,” PloS One, 8(5), p. e63141. [CrossRef] [PubMed]
Haynes, P., Nava, K. E., Lawson, B. A., Chung, C. S., Mitov, M. I., Campbell, S. G., Stromberg, A. J., Sadayappan, S., Bonnell, M. R., Hoopes, C. W., and Campbell, K. S., 2014, “Transmural Heterogeneity of Cellular Level Power Output is Reduced in Human Heart Failure,” J. Mol. Cell. Cardiol., 72, pp. 1–8. [CrossRef] [PubMed]
Mitov, M. I., Holbrook, A. M., and Campbell, K. S., 2009, “Myocardial Short-Range Force Responses Increase With Age in F344 Rats,” J. Mol. Cell. Cardiol., 46(1), pp. 39–46. [CrossRef] [PubMed]
Wenk, J. F., Sun, K., Zhang, Z., Soleimani, M., Ge, L., Saloner, D., Wallace, A. W., Ratcliffe, M. B., and Guccione, J. M., 2011, “Regional Left Ventricular Myocardial Contractility and Stress in a Finite Element Model of Posterobasal Myocardial Infarction,” ASME J. Biomech. Eng., 133(4), p. 044501. [CrossRef]
Guccione, J. M., McCulloch, A. D., and Waldman, L. K., 1991, “Passive Material Properties of Intact Ventricular Myocardium Determined From a Cylindrical Model,” ASME J. Biomech. Eng., 113(1), pp. 42–55. [CrossRef]
Jhun, C. S., Wenk, J. F., Zhang, Z., Wall, S. T., Sun, K., Sabbah, H. N., Ratcliffe, M. B., and Guccione, J. M., 2010, “Effect of Adjustable Passive Constraint on the Failing Left Ventricle: A Finite-Element Model Study,” Ann. Thorac. Surg., 89(1), pp. 132–137. [CrossRef] [PubMed]
Guccione, J. M., Waldman, L. K., and McCulloch, A. D., 1993, “Mechanics of Active Contraction in Cardiac Muscle: Part II–Cylindrical Models of the Systolic Left Ventricle,” ASME J. Biomech. Eng., 115(1), pp. 82–90. [CrossRef]
Lin, D. H., and Yin, F. C., 1998, “A Multiaxial Constitutive Law for Mammalian Left Ventricular Myocardium in Steady-State Barium Contracture or Tetanus,” ASME J. Biomech. Eng., 120(4), pp. 504–517. [CrossRef]
Walker, J. C., Ratcliffe, M. B., Zhang, P., Wallace, A. W., Fata, B., Hsu, E. W., Saloner, D., and Guccione, J. M., 2005, “MRI-Based Finite-Element Analysis of Left Ventricular Aneurysm,” Am. J. Physiol.: Heart Circ. Physiol., 289(2), pp. H692–H700. [CrossRef] [PubMed]
Guccione, J. M., Moonly, S. M., Moustakidis, P., Costa, K. D., Moulton, M. J., Ratcliffe, M. B., and Pasque, M. K., 2001, “Mechanism Underlying Mechanical Dysfunction in the Border Zone of Left Ventricular Aneurysm: A Finite Element Model Study,” Ann. Thorac. Surg., 71(2), pp. 654–662. [CrossRef] [PubMed]
Kerckhoffs, R. C., Neal, M. L., Gu, Q., Bassingthwaighte, J. B., Omens, J. H., and McCulloch, A. D., 2007, “Coupling of a 3D Finite Element Model of Cardiac Ventricular Mechanics to Lumped Systems Models of the Systemic and Pulmonic Circulation,” Ann. Biomed. Eng., 35(1), pp. 1–18. [CrossRef] [PubMed]
Watanabe, H., Sugiura, S., Kafuku, H., and Hisada, T., 2004, “Multiphysics Simulation of Left Ventricular Filling Dynamics Using Fluid-Structure Interaction Finite Element Method,” Biophys. J., 87(3), pp. 2074–2085. [CrossRef] [PubMed]
Healy, L. J., Jiang, Y., and Hsu, E. W., 2011, “Quantitative Comparison of Myocardial Fiber Structure Between Mice, Rabbit, and Sheep Using Diffusion Tensor Cardiovascular Magnetic Resonance,” J. Cardiovasc. Magn. Reson., 13(1), p. 74. [CrossRef] [PubMed]
Mekkaoui, C., Huang, S., Chen, H. H., Dai, G., Reese, T. G., Kostis, W. J., Thiagalingam, A., Maurovich-Horvat, P., Ruskin, J. N., Hoffmann, U., Jackowski, M. P., and Sosnovik, D. E., 2012, “Fiber Architecture in Remodeled Myocardium Revealed With a Quantitative Diffusion CMR Tractography Framework and Histological Validation,” J. Cardiovasc. Magn. Reson., 14(1), p. 70. [CrossRef] [PubMed]
Wang, Y., Zhang, K., Wasala, N. B., Yao, X., Duan, D., and Yao, G., 2014, “Histology Validation of Mapping Depth-Resolved Cardiac Fiber Orientation in Fresh Mouse Heart Using Optical Polarization Tractography,” Biomed. Opt. Express, 5(8), pp. 2843–2855. [CrossRef] [PubMed]
Scollan, D. F., Holmes, A., Winslow, R., and Forder, J., 1998, “Histological Validation of Myocardial Microstructure Obtained From Diffusion Tensor Magnetic Resonance Imaging,” Am. J. Physiol., 275(6), pp. H2308–H2318. [PubMed]
Wenk, J. F., Klepach, D., Lee, L. C., Zhang, Z., Ge, L., Tseng, E. E., Martin, A., Kozerke, S., Gorman, J. H., III, Gorman, R. C., and Guccione, J. M., 2012, “First Evidence of Depressed Contractility in the Border Zone of a Human Myocardial Infarction,” Ann. Thorac. Surg., 93(4), pp. 1188–1193. [CrossRef] [PubMed]
Nielsen, P. M., Le Grice, I. J., Smaill, B. H., and Hunter, P. J., 1991, “Mathematical Model of Geometry and Fibrous Structure of the Heart,” Am. J. Physiol., 260(4), pp. H1365–H1378. [PubMed]
Streeter, D., 1979, “Gross Morphology and Fiber Geometry of the Heart,” Handbook of Physiology, American Physiology Society, Bethesda, MD, pp. 61–112.
Russel, I. K., Gotte, M. J., Bronzwaer, J. G., Knaapen, P., Paulus, W. J., and van Rossum, A. C., 2009, “Left Ventricular Torsion: An Expanding Role in the Analysis of Myocardial Dysfunction,” JACC: Cardiovasc. Imaging, 2(5), pp. 648–655. [CrossRef] [PubMed]
Ingels, N. B., Hansen, D. E., Daughters, G. T., Stinson, E. B., Alderman, E. L., and Miller, D. C., 1989, “Relation Between Longitudinal, Circumferential, and Oblique Shortening and Torsional Deformation in the Left-Ventricle of the Transplanted Human-Heart,” Circ. Res., 64(5), pp. 915–927. [CrossRef] [PubMed]
Goffinet, C., Chenot, F., Robert, A., Pouleur, A. C., de Waroux, J. B. L., Vancrayenest, D., Gerard, O., Pasquet, A., Gerber, B. L., and Vanoverschelde, J. L., 2009, “Assessment of Subendocardial vs. Subepicardial Left Ventricular Rotation and Twist Using Two-Dimensional Speckle Tracking Echocardiography: Comparison With Tagged Cardiac Magnetic Resonance,” Eur. Heart J., 30(5), pp. 608–617. [CrossRef] [PubMed]

Figures

Grahic Jump Location
Fig. 1

A 3D FE model was created to simulate the function of LV. (a) Wireframe view of the LV, which was represented by an ellipsoidal morphology; (b) view with half of the model removed to show the LV wall with three transmural layers of equal thickness, outermost = epicardium, middle = midwall, and innermost = endocardium; (c) epicardial view of model with transmural variation in myofiber orientation (white lines within elements) and a radial–circumferential plane near the apex where the LV twist was assessed, and (d) example of the rotation angles of two specific nodes on the inner and outer surface of LV wall from end-diastolic to ES states.

Grahic Jump Location
Fig. 2

The transmural distribution of myocardium contractile strength altered the effects of myofiber orientation on the Starling relationship of LV. With the helical angle of epi-myofibers fixed at −30 deg, the effects of changes in endo-myofiber helical angle on the Starling curve of LV were assessed when Tmax for epi-, mid-, and endocardium was 150, 110, and 70 kPa, respectively, [case (i); (a)], and 70, 110, and 150 kPa, respectively, [case (ii); (b)]. The effects of epi-myofiber helical angle on LV Starling curve were assessed when the endo-myofibers were set at 60 deg for cases i (c) and ii (d), respectively.

Grahic Jump Location
Fig. 3

The transmural variations of myofiber orientation and contractile strength interdependently influenced the systolic twist angles of left ventricular apex. The apex twist angle of the LV from ED to ES was determined at EDP = 15 mmHg and ESP = 90 mmHg. The effects of endo-myofiber (a) and epi-myofiber (b) helical angles on LV apex twist were examined, respectively, for cases (i) and (ii).

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