Active contraction of cardiac muscle: in vivo characterization of mechanical activation sequences in the beating heart.

Progressive alterations in cardiac wall strains are a classic hallmark of chronic heart failure. Accordingly, the objectives of this study are to establish a baseline characterization of cardiac strains throughout the cardiac cycle, to quantify temporal, regional, and transmural variations of active fiber contraction, and to identify pathways of mechanical activation in the healthy beating heart. To this end, we insert two sets of twelve radiopaque beads into the heart muscle of nine sheep; one in the anterior-basal and one in the lateral-equatorial left ventricular wall. During three consecutive heartbeats, we record the bead coordinates via biplane videofluoroscopy. From the resulting four-dimensional data sets, we calculate the temporally and transmurally varying Green-Lagrange strains in the anterior and lateral wall. To quantify active contraction, we project the strains onto the local muscle fiber directions. We observe that mechanical activation is initiated at the endocardium slightly after end diastole and progresses transmurally outward, reaching the epicardium slightly before end systole. Accordingly, fibers near the outer wall are in contraction for approximately half of the cardiac cycle while fibers near the inner wall are in contraction almost throughout the entire cardiac cycle. In summary, cardiac wall strains display significant temporal, regional, and transmural variations. Quantifying wall strain profiles might be of particular clinical significance when characterizing stages of left ventricular remodeling, but also of engineering relevance when designing new biomaterials of similar structure and function.

[1]  D. Mozaffarian,et al.  Heart disease and stroke statistics--2010 update: a report from the American Heart Association. , 2010, Circulation.

[2]  Bernd Hertenstein,et al.  Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial , 2004, The Lancet.

[3]  Serdar Göktepe,et al.  Electromechanics of Cardiac Tissue: A Unified Approach to the Fully Coupled Excitation‐Contraction Problem , 2009 .

[4]  S. Göktepe,et al.  Computational modeling of passive myocardium , 2011 .

[5]  A. McCulloch,et al.  Relating myocardial laminar architecture to shear strain and muscle fiber orientation. , 2001, American journal of physiology. Heart and circulatory physiology.

[6]  Frank Langer,et al.  Transmural cardiac strains in the lateral wall of the ovine left ventricle. , 2005, American journal of physiology. Heart and circulatory physiology.

[7]  Peter Gaudron,et al.  Progressive Left Ventricular Dysfunction and Remodeling After Myocardial Infarction Potential Mechanisms and Early Predictors , 1993, Circulation.

[8]  A. Schwarzkopf,et al.  A comparison of two analytical systems for 3-D reconstruction from biplane videoradiograms , 1988, Proceedings. Computers in Cardiology 1988.

[9]  Serdar Göktepe,et al.  In-Vivo Dynamic Strains of the Ovine Anterior Mitral Valve Leaflet , 2011 .

[10]  Andrew D McCulloch,et al.  Laminar fiber architecture and three-dimensional systolic mechanics in canine ventricular myocardium. , 1999, American journal of physiology. Heart and circulatory physiology.

[11]  Neil B. Ingels,et al.  Characterization of Mitral Valve Annular Dynamics in the Beating Heart , 2011, Annals of Biomedical Engineering.

[12]  S. Göktepe,et al.  Computational modeling of electrocardiograms: A finite element approach toward cardiac excitation , 2010 .

[13]  Serdar Göktepe,et al.  A multiscale model for eccentric and concentric cardiac growth through sarcomerogenesis. , 2010, Journal of theoretical biology.

[14]  Daniel B Ennis,et al.  Myofiber angle distributions in the ovine left ventricle do not conform to computationally optimized predictions. , 2008, Journal of biomechanics.

[15]  R M Norris,et al.  Progressive left ventricular dysfunction and remodeling after myocardial infarction. , 1994, Circulation.

[16]  Frank Langer,et al.  Transmural sheet strains in the lateral wall of the ovine left ventricle. , 2005, American journal of physiology. Heart and circulatory physiology.

[17]  S. Göktepe,et al.  Electromechanics of the heart: a unified approach to the strongly coupled excitation–contraction problem , 2010 .

[18]  M Karlsson,et al.  Transmural strains in the ovine left ventricular lateral wall during diastolic filling. , 2009, Journal of biomechanical engineering.

[19]  W. Yeong,et al.  Engineering functionally graded tissue engineering scaffolds. , 2008, Journal of the mechanical behavior of biomedical materials.

[20]  Ellen Kuhl,et al.  IN VITRO/IN SILICO CHARACTERIZATION OF ACTIVE AND PASSIVE STRESSES IN CARDIAC MUSCLE , 2012 .

[21]  Serdar Göktepe,et al.  A generic approach towards finite growth with examples of athlete's heart, cardiac dilation, and cardiac wall thickening , 2010 .

[22]  G A Klassen,et al.  Transmural myocardial deformation in the canine left ventricular wall. , 1978, The American journal of physiology.

[23]  Kevin D Costa,et al.  Contribution of laminar myofiber architecture to load-dependent changes in mechanics of LV myocardium. , 2002, American journal of physiology. Heart and circulatory physiology.

[24]  M A Niczyporuk,et al.  Automatic tracking and digitization of multiple radiopaque myocardial markers. , 1991, Computers and biomedical research, an international journal.

[25]  S. Göktepe,et al.  Atrial and ventricular fibrillation: computational simulation of spiral waves in cardiac tissue , 2010 .

[26]  A. McCulloch,et al.  Non-homogeneous analysis of three-dimensional transmural finite deformation in canine ventricular myocardium. , 1991, Journal of biomechanics.

[27]  Daniel B. Ennis,et al.  Alterations in Transmural Myocardial Strain: An Early Marker of Left Ventricular Dysfunction in Mitral Regurgitation? , 2008, Circulation.

[28]  Andrew D McCulloch,et al.  Asynchrony of ventricular activation affects magnitude and timing of fiber stretch in late-activated regions of the canine heart. , 2007, American journal of physiology. Heart and circulatory physiology.

[29]  Olga Solovyova,et al.  Influence of viscosity on myocardium mechanical activity: a mathematical model. , 2004, Journal of theoretical biology.

[30]  D. Durrer,et al.  Total Excitation of the Isolated Human Heart , 1970, Circulation.

[31]  P. McCarthy,et al.  Reverse ventricular remodeling: mechanical options , 2006, Current opinion in cardiology.

[32]  Y. Fung,et al.  Transmural Myocardial Deformation in the Canine Left Ventricle: Normal in Vivo Three‐Dimensional Finite Strains , 1985, Circulation research.

[33]  Markus Böl,et al.  Computational modeling of muscular thin films for cardiac repair , 2009 .

[34]  A. Cheng,et al.  Heterogeneity of Left Ventricular Wall Thickening Mechanisms , 2008, Circulation.

[35]  M Karlsson,et al.  Nonhomogeneous strain from sparse marker arrays for analysis of transmural myocardial mechanics. , 2007, Journal of biomechanical engineering.

[36]  Neil B. Ingels,et al.  Passive Ventricular Constraint Prevents Transmural Shear Strain Progression in Left Ventricle Remodeling , 2006, Circulation.

[37]  Daniel B Ennis,et al.  Transmural left ventricular shear strain alterations adjacent to and remote from infarcted myocardium. , 2006, The Journal of heart valve disease.

[38]  Randall J Lee,et al.  Biomaterials for the treatment of myocardial infarction. , 2006, Journal of the American College of Cardiology.