Material properties of the ovine mitral valve anterior leaflet in vivo from inverse finite element analysis.

We measured leaflet displacements and used inverse finite-element analysis to define, for the first time, the material properties of mitral valve (MV) leaflets in vivo. Sixteen miniature radiopaque markers were sewn to the MV annulus, 16 to the anterior MV leaflet, and 1 on each papillary muscle tip in 17 sheep. Four-dimensional coordinates were obtained from biplane videofluoroscopic marker images (60 frames/s) during three complete cardiac cycles. A finite-element model of the anterior MV leaflet was developed using marker coordinates at the end of isovolumic relaxation (IVR; when the pressure difference across the valve is approximately 0), as the minimum stress reference state. Leaflet displacements were simulated during IVR using measured left ventricular and atrial pressures. The leaflet shear modulus (G(circ-rad)) and elastic moduli in both the commisure-commisure (E(circ)) and radial (E(rad)) directions were obtained using the method of feasible directions to minimize the difference between simulated and measured displacements. Group mean (+/-SD) values (17 animals, 3 heartbeats each, i.e., 51 cardiac cycles) were as follows: G(circ-rad) = 121 +/- 22 N/mm2, E(circ) = 43 +/- 18 N/mm2, and E(rad) = 11 +/- 3 N/mm2 (E(circ) > E(rad), P < 0.01). These values, much greater than those previously reported from in vitro studies, may result from activated neurally controlled contractile tissue within the leaflet that is inactive in excised tissues. This could have important implications, not only to our understanding of mitral valve physiology in the beating heart but for providing additional information to aid the development of more durable tissue-engineered bioprosthetic valves.

[1]  Smith Rb Intrinsic innervation of the atrioventricular and semilunar valves in various mammals. , 1971 .

[2]  F. Yin,et al.  Biaxial mechanical behavior of excised porcine mitral valve leaflets. , 1995, The American journal of physiology.

[3]  T. H. Williams MITRAL AND TRICUSPID VALVE INNERVATION , 1964, British heart journal.

[4]  E. Sonnenblick,et al.  An Intrinsic Neuromuscular Basis for Mitral Valve Motion in the Dog , 1967, Circulation research.

[5]  A. L. Wit,et al.  Electrophysiological Properties of Cardiac Muscle in the Anterior Mitral Valve Leaflet and the Adjacent Atrium in the Dog: POSSIBLE IMPLICATIONS FOR THE GENESIS OF ATRIAL DYSRHYTHMIAS , 1973, Circulation research.

[6]  Andrew L. Wit,et al.  Canine Mitral Complex: ULTRASTRUCTURE AND ELECTROMECHANICAL PROPERTIES , 1972, Circulation research.

[7]  A. L. Wit,et al.  Ultrastructure and Transmembrane Potentials of Cardiac Muscle in the Human Anterior Mitral Valve Leaflet , 1979, Circulation.

[8]  M. Simionescu,et al.  Interstitial Cells of the Heart Valves Possess Characteristics Similar to Smooth Muscle Cells , 1986, Circulation research.

[9]  P. Dagum,et al.  Ablation of mitral annular and leaflet muscle: effects on annular and leaflet dynamics. , 2003, American journal of physiology. Heart and circulatory physiology.

[10]  K. J. Grande-Allen,et al.  Glycosaminoglycans and proteoglycans in normal mitral valve leaflets and chordae: association with regions of tensile and compressive loading. , 2004, Glycobiology.

[11]  D. Ghista,et al.  Structural mechanics of the mitral valve: stresses sustained by the valve; non-traumatic determination of the stiffness of the in vivo valve. , 1972, Journal of biomechanics.

[12]  Ashok D. Belegundu,et al.  Parallel Line Search in Method of Feasible Directions , 2004 .

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

[14]  K S Kunzelman,et al.  Nondestructive analysis of mitral valve collagen fiber orientation. , 1991, ASAIO transactions.

[15]  R. B. Smith Intrinsic innervation of the atrioventricular and semilunar valves in various mammals. , 1971, Journal of anatomy.

[16]  T Cooper,et al.  Structural basis of cardiac valvar function. , 1966, Archives of surgery.

[17]  R. Hibbs,et al.  The atrioventricular valves of the guinea-pig. II. An ultrastructural study. , 1973, The American journal of anatomy.

[18]  Mark Eastwood,et al.  Force generation of different human cardiac valve interstitial cells: relevance to individual valve function and tissue engineering. , 2007, The Journal of heart valve disease.

[19]  W. S. Ring,et al.  Finite element analysis of the mitral valve. , 1993, The Journal of heart valve disease.

[20]  S. Kawai,et al.  Morphological study on vagal innervation in human atrioventricular valves using histochemical method. , 1993, Japanese circulation journal.

[21]  W. Lipp,et al.  The adrenergic nerve plexuses of cardiac valves. , 1968, Acta Anatomica.

[22]  S. Ito,et al.  Histopathologic studies of innervation of normal and prolapsed human mitral valves. , 1995, The Journal of heart valve disease.

[23]  J. Jew,et al.  Is the mitral valve passive flap theory overstated? An active valve is hypothesized. , 2004, Medical hypotheses.

[24]  R Haaverstad,et al.  Finite element analysis of the mitral apparatus: annulus shape effect and chordal force distribution , 2009, Biomechanics and modeling in mechanobiology.

[25]  O. Johansson,et al.  Distribution of PGP 9.5, TH, NPY, SP and CGRP immunoreactive nerves in the rat and guinea pig atrioventricular valves and chordae tendineae , 1997, Journal of anatomy.

[26]  R. P. Cochran,et al.  Fluid–structure interaction models of the mitral valve: function in normal and pathological states , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[27]  R. P. Cochran,et al.  Mechanical properties of basal and marginal mitral valve chordae tendineae. , 1990, ASAIO transactions.

[28]  A. Chester,et al.  Molecular and functional characteristics of heart-valve interstitial cells , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[29]  Joon Hock Yeo,et al.  Three-dimensional asymmetrical modeling of the mitral valve: a finite element study with dynamic boundaries. , 2005, The Journal of heart valve disease.

[30]  D. C. Miller,et al.  Effect of cutting second-order chordae on in-vivo anterior mitral leaflet compound curvature. , 2005, The Journal of heart valve disease.

[31]  Karen May-Newman,et al.  The structure and mechanical properties of the mitral valve leaflet-strut chordae transition zone. , 2004, Journal of biomechanical engineering.

[32]  R. Anderson,et al.  The disposition and innervation of atrioventricular ring specialized tissue in rats and rabbits. , 1972, Journal of anatomy.

[33]  R. Hibbs,et al.  The atrioventricular valves of the guinea-pig. I. A light microscopic study. , 1973, The American journal of anatomy.

[34]  T. Cooper,et al.  Electrical activity of the canine mitral valve in situ. , 1969, The American journal of physiology.

[35]  J. Jew,et al.  Tyrosine hydroxylase- and nitric oxide synthase-immunoreactive nerve fibers in mitral valve of young adult and aged Fischer 344 rats. , 1996, Journal of the autonomic nervous system.

[36]  Anderson Rh,et al.  The disposition and innervation of atrioventricular ring specialized tissue in rats and rabbits. , 1972 .

[37]  F. Bowen,et al.  Effect of Annular Shape on Leaflet Curvature in Reducing Mitral Leaflet Stress , 2002, Circulation.

[38]  A. McCulloch,et al.  Nonhomogeneous Deformation in the Anterior Leaflet of the Mitral Valve , 2004, Annals of Biomedical Engineering.

[39]  A. L. Wit,et al.  Triggered Activity in Cardiac Muscle Fibers of the Simian Mitral Valve , 1976, Circulation research.

[40]  Ajit P Yoganathan,et al.  Effects of papillary muscle position on in-vitro dynamic strain on the porcine mitral valve. , 2003, The Journal of heart valve disease.

[41]  J Günter Grossmann,et al.  Collagen organization in canine myxomatous mitral valve disease: an x-ray diffraction study. , 2007, Biophysical journal.

[42]  R. E. Clark,et al.  Stress-strain characteristics of fresh and frozen human aortic and mitral leaflets and chordae tendineae. Implications for clinical use. , 1973, The Journal of thoracic and cardiovascular surgery.

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

[44]  S. Biasi,et al.  Histochemical and ultrastructural study on the innervation of human and porcine atrio-ventricular valves , 2004, Anatomy and Embryology.

[45]  D. C. Miller,et al.  Altered mitral valve kinematics with atrioventricular and ventricular pacing. , 2005, Journal of Heart Valve Disease.

[46]  Filip Da Mouse atrio-ventricular valve ultrastructure morphometrical correlations. , 1984 .

[47]  T. Williams,et al.  Variations in atrioventricular valve innervation in four species of mammals. , 1990, The American journal of anatomy.

[48]  A. Yoganathan,et al.  In-vivo dynamic deformation of the mitral valve anterior leaflet. , 2006, The Annals of thoracic surgery.

[49]  A. Yoganathan,et al.  Heart valve function: a biomechanical perspective , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[50]  T. Kundu,et al.  Distribution of the microelastic properties within the human anterior mitral leaflet. , 2006, Ultrasound in medicine & biology.

[51]  Masashi Komeda,et al.  Mitral valve opening in the ovine heart. , 1998, American journal of physiology. Heart and circulatory physiology.

[52]  Magdi H. Yacoub,et al.  Localization and pattern of expression of extracellular matrix components in human heart valves. , 2005, The Journal of heart valve disease.

[53]  J. Marshall,et al.  Three-dimensional echocardiographic reconstruction of the mitral valve, with implications for the diagnosis of mitral valve prolapse. , 1989, Circulation.

[54]  P. McCarthy,et al.  Mitral valve stiffening in end-stage heart failure: evidence of an organic contribution to functional mitral regurgitation. , 2005, The Journal of thoracic and cardiovascular surgery.

[55]  R. P. Cochran,et al.  Stress/Strain Characteristics of Porcine Mitral Valve Tissue: Parallel Versus Perpendicular Collagen Orientation , 1992, Journal of cardiac surgery.

[56]  K S Kunzelman,et al.  The effect of chordal replacement suture length on function and stresses in repaired mitral valves: a finite element study. , 1996, The Journal of heart valve disease.

[57]  Ajit P Yoganathan,et al.  A saddle-shaped annulus reduces systolic strain on the central region of the mitral valve anterior leaflet. , 2007, The Journal of thoracic and cardiovascular surgery.

[58]  K. May-Newman,et al.  Effect of Strut Chordae Transection on Mitral Valve Leaflet Biomechanics , 2006, Annals of Biomedical Engineering.

[59]  Alberto Redaelli,et al.  An annular prosthesis for the treatment of functional mitral regurgitation: finite element model analysis of a dog bone-shaped ring prosthesis. , 2005, The Annals of thoracic surgery.

[60]  T. H. Williams FAST-CONDUCTING FIBRES IN THE MITRAL VALVE , 1964, British heart journal.