© 1995 American Heart Association, Inc.
Articles |
Transverse Shear Along Myocardial Cleavage Planes Provides a Mechanism for Normal Systolic Wall Thickening
From the Division of Cardiology, Department of Medicine, University of California, San Diego (La Jolla).
Correspondence to James W Covell, MD, BSB 2004-0613J, UC San Diego, 9500 Gilman Dr, La Jolla, CA 92093.
Abstract Recent studies in humans and other species show that there is substantial transverse shear strain in the left ventricular myocardium, and others have shown transverse myocardial laminae separated by cleavage planes. We proposed that cellular rearrangement based on shearing along myocardial cleavage planes could account for >50% of normal systolic wall thickening, since <50% can be explained by increases in myocyte diameter. To test this hypothesis, we measured strains at two sites with different cleavage-plane anatomy in eight open-chest dogs. Columns of radiopaque markers were implanted in the left ventricular anterior free wall and septum. Markers were tracked with biplane cineradiography, and strains were quantified by using finite deformation techniques. Hearts were perfusion-fixed with glutaraldehyde, and cleavage-plane orientations at the bead sites were measured in three orthogonal planes. At subendocardial sites of the anterior left ventricular wall, where the cleavage planes approach the endocardium obliquely from the apical side of the surface normal in the longitudinal-radial plane (-67±11°), systolic longitudinal-radial transverse shear (E23) was positive (0.14±0.08). At the septal sites where the subendocardial cleavage planes approach the endocardium obliquely from above the surface normal (44±12°), E23 was negative (-0.12±0.08). The differences in cleavage-plane angle and E23 at the two sites were each highly significant (P<.0005). At both sites, the transverse shear strain accompanied substantial systolic wall thickening at the subendocardium (anterior, E33=0.44±0.16; septum, E33=0.22±0.14). These data are not representative of the behavior in midwall and outer wall sites, where cleavage-plane orientation was not consistently different between anterior left ventricle and septum. Our data indicate that rearrangement of myocytes by slippage along myocardial cleavage planes is in the correct direction and of sufficient magnitude in the subendocardium (inner third) to account for a substantial proportion (>50%) of systolic wall thickening. Furthermore, three-dimensional reconstruction of the myocardial laminae and local comparison with maximum strain vectors indicate that for the inner third of the ventricular wall the maximum shear deformation is a result of relative sliding between myocardial laminae.
Key Words: laminar myocardium • myocardial mechanics
This article has been cited by other articles:
 |
|
 |
|
  F. Dorri, P. F. Niederer, P. P. Lunkenheimer, and R. H. Anderson The architecture of the left ventricular myocytes relative to left ventricular systolic function Eur. J. Cardiothorac. Surg., February 1, 2010; 37(2): 384 - 392. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Ishizu, Y. Seo, Y. Enomoto, H. Sugimori, M. Yamamoto, T. Machino, R. Kawamura, and K. Aonuma Experimental validation of left ventricular transmural strain gradient with echocardiographic two-dimensional speckle tracking imaging Eur J Echocardiogr, January 6, 2010; (2010) jep221v1. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. P. H. M. van den Wijngaard, P. van Horssen, R. ter Wee, R. Coronel, J. M. de Bakker, N. de Jonge, M. Siebes, and J. A. E. Spaan Organization and collateralization of a subendocardial plexus in end-stage human heart failure Am J Physiol Heart Circ Physiol, January 1, 2010; 298(1): H158 - H162. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. J. Caldwell, M. L. Trew, G. B. Sands, D. A. Hooks, I. J. LeGrice, and B. H. Smaill Three Distinct Directions of Intramural Activation Reveal Nonuniform Side-to-Side Electrical Coupling of Ventricular Myocytes Circ Arrhythm Electrophysiol, August 1, 2009; 2(4): 433 - 440. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Nasiraei-Moghaddam and M. Gharib Evidence for the existence of a functional helical myocardial band Am J Physiol Heart Circ Physiol, January 1, 2009; 296(1): H127 - H131. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 O. Gjesdal, T. Helle-Valle, E. Hopp, K. Lunde, T. Vartdal, S. Aakhus, H.-J. Smith, H. Ihlen, and T. Edvardsen Noninvasive Separation of Large, Medium, and Small Myocardial Infarcts in Survivors of Reperfused ST-Elevation Myocardial Infarction: A Comprehensive Tissue Doppler and Speckle-Tracking Echocardiography Study Circ Cardiovasc Imaging, November 1, 2008; 1(3): 189 - 196. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. J. Pope, G. B. Sands, B. H. Smaill, and I. J. LeGrice Three-dimensional transmural organization of perimysial collagen in the heart Am J Physiol Heart Circ Physiol, September 1, 2008; 295(3): H1243 - H1252. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. W. Covell Tissue Structure and Ventricular Wall Mechanics Circulation, August 12, 2008; 118(7): 699 - 701. [Full Text] [PDF]
|
|
|
|
|
|
A. Cheng, T. C. Nguyen, M. Malinowski, G. T. Daughters, D. C. Miller, and N. B. Ingels Jr Heterogeneity of Left Ventricular Wall Thickening Mechanisms Circulation, August 12, 2008; 118(7): 713 - 721. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Ashikaga, B. A. Coppola, K. G. Yamazaki, F. J. Villarreal, J. H. Omens, and J. W. Covell Changes in regional myocardial volume during the cardiac cycle: implications for transmural blood flow and cardiac structure Am J Physiol Heart Circ Physiol, August 1, 2008; 295(2): H610 - H618. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. H. Gilbert, A. P. Benson, P. Li, and A. V. Holden Regional localisation of left ventricular sheet structure: integration with current models of cardiac fibre, sheet and band structure Eur. J. Cardiothorac. Surg., August 1, 2007; 32(2): 231 - 249. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. P. Sengupta, J. Korinek, M. Belohlavek, J. Narula, M. A. Vannan, A. Jahangir, and B. K. Khandheria Left Ventricular Structure and Function: Basic Science for Cardiac Imaging J. Am. Coll. Cardiol., November 21, 2006; 48(10): 1988 - 2001. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Kostelec, J. Covell, G. D. Buckberg, A. Sadeghi, J. I.E. Hoffman, and G. S. Kassab Myocardial protection in the failing heart: I. Effect of cardioplegia and the beating state under simulated left ventricular restoration J. Thorac. Cardiovasc. Surg., October 1, 2006; 132(4): 875 - 883. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. S. Kassab, M. Kostelec, G. D. Buckberg, J. Covell, A. Sadeghi, and J. I.E. Hoffman Myocardial protection in the failing heart: II. Effect of pulsatile cardioplegic perfusion under simulated left ventricular restoration J. Thorac. Cardiovasc. Surg., October 1, 2006; 132(4): 884 - 890. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Cheng, T. C. Nguyen, M. Malinowski, D. Liang, G. T. Daughters, N. B. Ingels Jr, and D. C. Miller Effects of Undersized Mitral Annuloplasty on Regional Transmural Left Ventricular Wall Strains and Wall Thickening Mechanisms Circulation, July 4, 2006; 114(1_suppl): I-600 - I-609. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Coghlan and J. Hoffman Leonardo da Vinci's flights of the mind must continue: cardiac architecture and the fundamental relation of form and function revisited Eur. J. Cardiothorac. Surg., April 1, 2006; 29(Suppl_1): S4 - S17. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. J. Kocica, A. F. Corno, F. Carreras-Costa, M. Ballester-Rodes, M. C. Moghbel, C. N.C. Cueva, V. Lackovic, V. I. Kanjuh, and F. Torrent-Guasp The helical ventricular myocardial band: global, three-dimensional, functional architecture of the ventricular myocardium Eur. J. Cardiothorac. Surg., April 1, 2006; 29(Suppl_1): S21 - S40. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. D. Buckberg, M. Castella, M. Gharib, and S. Saleh Structure/function interface with sequential shortening of basal and apical components of the myocardial band Eur. J. Cardiothorac. Surg., April 1, 2006; 29(Suppl_1): S75 - S97. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. D. Buckberg, M. Castella, M. Gharib, and S. Saleh Active myocyte shortening during the 'isovolumetric relaxation' phase of diastole is responsible for ventricular suction; 'systolic ventricular filling' Eur. J. Cardiothorac. Surg., April 1, 2006; 29(Suppl_1): S98 - S106. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Ballester-Rodes, A. Flotats, F. Torrent-Guasp, I. Carrio-Gasset, M. Ballester-Alomar, F. Carreras, A. Ferreira, and J. Narula The sequence of regional ventricular motion Eur. J. Cardiothorac. Surg., April 1, 2006; 29(Suppl_1): S139 - S144. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. L. Trew, B. J. Caldwell, G. B. Sands, D. A. Hooks, D. C.-S. Tai, T. M. Austin, I. J. LeGrice, A. J. Pullan, and B. H. Smaill Cardiac electrophysiology and tissue structure: bridging the scale gap with a joint measurement and modelling paradigm Exp Physiol, March 1, 2006; 91(2): 355 - 370. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. D. McCulloch and J. H. Omens Myocyte Shearing, Myocardial Sheets, and Microtubules Circ. Res., January 6, 2006; 98(1): 1 - 3. [Full Text] [PDF]
|
|
|
|
|
|
S. Nishimura, S. Nagai, M. Katoh, H. Yamashita, Y. Saeki, J.-i. Okada, T. Hisada, R. Nagai, and S. Sugiura Microtubules Modulate the Stiffness of Cardiomyocytes Against Shear Stress Circ. Res., January 6, 2006; 98(1): 81 - 87. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Chen, W. Liu, H. Zhang, L. Lacy, X. Yang, S.-K. Song, S. A. Wickline, and X. Yu Regional ventricular wall thickening reflects changes in cardiac fiber and sheet structure during contraction: quantification with diffusion tensor MRI Am J Physiol Heart Circ Physiol, November 1, 2005; 289(5): H1898 - H1907. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Cheng, F. Langer, F. Rodriguez, J. C. Criscione, G. T. Daughters, D. C. Miller, and N. B. Ingels Jr. Transmural sheet strains in the lateral wall of the ovine left ventricle Am J Physiol Heart Circ Physiol, September 1, 2005; 289(3): H1234 - H1241. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Cheng, F. Langer, F. Rodriguez, J. C. Criscione, G. T. Daughters, D. C. Miller, and N. B. Ingels Jr. Transmural cardiac strains in the lateral wall of the ovine left ventricle Am J Physiol Heart Circ Physiol, April 1, 2005; 288(4): H1546 - H1556. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. B. Harrington, F. Rodriguez, A. Cheng, F. Langer, H. Ashikaga, G. T. Daughters, J. C. Criscione, N. B. Ingels, and D. C. Miller Direct measurement of transmural laminar architecture in the anterolateral wall of the ovine left ventricle: new implications for wall thickening mechanics Am J Physiol Heart Circ Physiol, March 1, 2005; 288(3): H1324 - H1330. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Torrent-Guasp, M. J. Kocica, A. F. Corno, M. Komeda, F. Carreras-Costa, A. Flotats, J. Cosin-Aguillar, and H. Wen Towards new understanding of the heart structure and function Eur. J. Cardiothorac. Surg., February 1, 2005; 27(2): 191 - 201. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 U. Rueckschloss and G. Isenberg Contraction augments L-type Ca2+ currents in adherent guinea-pig cardiomyocytes J. Physiol., October 15, 2004; 560(2): 403 - 411. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. D. Buckberg, M. L. Weisfeldt, M. Ballester, R. Beyar, D. Burkhoff, H. C. Coghlan, M. Doyle, N. D. Epstein, M. Gharib, R. E. Ideker, et al. Left Ventricular Form and Function: Scientific Priorities and Strategic Planning for Development of New Views of Disease Circulation, October 5, 2004; 110(14): e333 - e336. [Full Text] [PDF]
|
|
|
|
|
|
H. Ashikaga, J. H. Omens, N. B. Ingels Jr., and J. W. Covell Transmural mechanics at left ventricular epicardial pacing site Am J Physiol Heart Circ Physiol, June 1, 2004; 286(6): H2401 - H2407. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Yalcin, H. Muderrisoglu, M. E. Korkmaz, B. Ozin, M. Baltali, and F. Yigit The Effect of Dobutamine Stress on Left Ventricular Outflow Tract Gradients in Hypertensive Patients with Basal Septal Hypertrophy Angiology, May 1, 2004; 55(3): 295 - 301. [Abstract] [PDF]
|
|
|
|
|
|
F. Torrent-Guasp, M. J. Kocica, A. Corno, M. Komeda, J. Cox, A. Flotats, M. Ballester-Rodes, and F. Carreras-Costa Systolic ventricular filling Eur. J. Cardiothorac. Surg., March 1, 2004; 25(3): 376 - 386. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Ashikaga, J. C. Criscione, J. H. Omens, J. W. Covell, and N. B. Ingels Jr. Transmural left ventricular mechanics underlying torsional recoil during relaxation Am J Physiol Heart Circ Physiol, February 1, 2004; 286(2): H640 - H647. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Dokos, B. H. Smaill, A. A. Young, and I. J. LeGrice Shear properties of passive ventricular myocardium Am J Physiol Heart Circ Physiol, December 1, 2002; 283(6): H2650 - H2659. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Sussman, A. McCulloch, and T. K. Borg Dance Band on the Titanic: Biomechanical Signaling in Cardiac Hypertrophy Circ. Res., November 15, 2002; 91(10): 888 - 898. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. J. Sinusas, X. Papademetris, R. T. Constable, D. P. Dione, M. D. Slade, P. Shi, and J. S. Duncan Quantification of 3-D regional myocardial deformation: shape-based analysis of magnetic resonance images Am J Physiol Heart Circ Physiol, August 1, 2001; 281(2): H698 - H714. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Mazhari, J. H. Omens, R. S. Pavelec, J. W. Covell, and A. D. McCulloch Transmural Distribution of Three-Dimensional Systolic Strains in Stunned Myocardium Circulation, July 17, 2001; 104(3): 336 - 341. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Arts, K. D. Costa, J. W. Covell, and A. D. McCulloch Relating myocardial laminar architecture to shear strain and muscle fiber orientation Am J Physiol Heart Circ Physiol, May 1, 2001; 280(5): H2222 - H2229. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. M. Shoucri Active and passive stresses in the myocardium Am J Physiol Heart Circ Physiol, November 1, 2000; 279(5): H2519 - H2528. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Tobita and B. B. Keller Right and left ventricular wall deformation patterns in normal and left heart hypoplasia chick embryos Am J Physiol Heart Circ Physiol, September 1, 2000; 279(3): H959 - H969. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Mazhari, J. H Omens, J. W Covell, and A. D McCulloch Structural basis of regional dysfunction in acutely ischemic myocardium Cardiovasc Res, August 1, 2000; 47(2): 284 - 293. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 W.-Y. I. Tseng, T. G. Reese, R. M. Weisskoff, T. J. Brady, and V. J. Wedeen Myocardial Fiber Shortening in Humans: Initial Results of MR Imaging Radiology, July 1, 2000; 216(1): 128 - 139. [Abstract] [Full Text]
|
|
|
|
|
|
J. Bogaert, H. Bosmans, A. Maes, P. Suetens, G. Marchal, and F. E. Rademakers Remote myocardial dysfunction after acute anterior myocardial infarction: impact of left ventricular shape on regional function: A magnetic resonance myocardial tagging study J. Am. Coll. Cardiol., May 1, 2000; 35(6): 1525 - 1534. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S.-J. Dong, P. S. Hees, W.-M. Huang, S. A. Buffer Jr., J. L. Weiss, and E. P. Shapiro Independent effects of preload, afterload, and contractility on left ventricular torsion Am J Physiol Heart Circ Physiol, September 1, 1999; 277(3): H1053 - H1060. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. D. Costa, Y. Takayama, A. D. McCulloch, and J. W. Covell Laminar fiber architecture and three-dimensional systolic mechanics in canine ventricular myocardium Am J Physiol Heart Circ Physiol, February 1, 1999; 276(2): H595 - H607. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. F. Scollan, A. Holmes, R. Winslow, and J. Forder Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging Am J Physiol Heart Circ Physiol, December 1, 1998; 275(6): H2308 - H2318. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. W. Hsu, A. L. Muzikant, S. A. Matulevicius, R. C. Penland, and C. S. Henriquez Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation Am J Physiol Heart Circ Physiol, May 1, 1998; 274(5): H1627 - H1634. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. D. Costa, K. May-Newman, D. Farr, W. G. O'Dell, A. D. McCulloch, and J. H. Omens Three-dimensional residual strain in midanterior canine left ventricle Am J Physiol Heart Circ Physiol, October 1, 1997; 273(4): H1968 - H1976. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. A. MacGowan, E. P. Shapiro, H. Azhari, C. O. Siu, P. S. Hees, G. M. Hutchins, J. L. Weiss, and F. E. Rademakers Noninvasive Measurement of Shortening in the Fiber and Cross-Fiber Directions in the Normal Human Left Ventricle and in Idiopathic Dilated Cardiomyopathy Circulation, July 15, 1997; 96(2): 535 - 541. [Abstract] [Full Text]
|
|
|
|
|
|
Y. Takayama, K. D. Costa, and J. W. Covell Contribution of laminar myofiber architecture to load-dependent changes in mechanics of LV myocardium Am J Physiol Heart Circ Physiol, April 1, 2002; 282(4): H1510 - H1520. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. H. Omens, T. P. Usyk, Z. Li, and A. D. McCulloch Muscle LIM protein deficiency leads to alterations in passive ventricular mechanics Am J Physiol Heart Circ Physiol, February 1, 2002; 282(2): H680 - H687. [Abstract] [Full Text] [PDF]
|
|