Trabeculae carneae account for a significant portion of human ventricular mass, despite being considered embryologic remnants. Recent studies have found trabeculae hypertrophy and fibrosis in hypertrophied left ventricles with various pathological conditions. The objective of this study was to investigate the passive mechanical properties and microstructural characteristics of trabeculae carneae and papillary muscles compared to the myocardium in human hearts. Uniaxial tensile tests were performed on samples of trabeculae carneae and myocardium strips, while biaxial tensile tests were performed on samples of papillary muscles and myocardium sheets. The experimental data were fitted with a Fung-type strain energy function and material coefficients were determined. The secant moduli at given diastolic stress and strain levels were determined and compared among the tissues. Following the mechanical testing, histology examinations were performed to investigate the microstructural characteristics of the tissues. Our results demonstrated that the trabeculae carneae were significantly stiffer (Secant modulus SM2 = 80.06 ± 10.04 KPa) and had higher collagen content (16.10 ± 3.80%) than the myocardium (SM2 = 55.14 ± 20.49 KPa, collagen content = 10.06 ± 4.15%) in the left ventricle. The results of this study improve our understanding of the contribution of trabeculae carneae to left ventricular compliance and will be useful for building accurate computational models of the human heart.
References
1.
Yancy
, C. W.
, Jessup
, M.
, Bozkurt
, B.
, Butler
, J.
, Casey
, D. E.
, Drazner
, M. H.
, Fonarow
, G. C.
, Geraci
, S. A.
, Horwich
, T.
, Januzzi
, J. L.
, Johnson
, M. R.
, Kasper
, E. K.
, Levy
, W. C.
, Masoudi
, F. A.
, McBride
, P. E.
, McMurray
, J. J. V.
, Mitchell
, J. E.
, Peterson
, P. N.
, Riegel
, B.
, Sam
, F.
, Stevenson
, L. W.
, Tang
, W. H. W.
, Tsai
, E. J.
, and Wilkoff
, B. L.
, 2013
, “2013 ACCF/AHA Guideline for the Management of Heart Failure: A Report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines
,” Circulation
, 128
(16
), pp. e240
–e327
.2.
Dhingra
, A.
, Garg
, A.
, Kaur
, S.
, Chopra
, S.
, Batra
, J. S.
, Pandey
, A.
, Chaanine
, A. H.
, and Agarwal
, S. K.
, 2014
, “Epidemiology of Heart Failure With Preserved Ejection Fraction
,” Curr. Heart Failure Rep.
, 11
(4
), pp. 354
–365
.3.
Owan
, T. E.
, Hodge
, D. O.
, Herges
, R. M.
, Jacobsen
, S. J.
, Roger
, V. L.
, and Redfield
, M. M.
, 2006
, “Trends in Prevalence and Outcome of Heart Failure With Preserved Ejection Fraction
,” New Engl. J. Med.
, 355
(3
), pp. 251
–259
.4.
LeWinter
, M. M.
, and Meyer
, M.
, 2013
, “Mechanisms of Diastolic Dysfunction in HFpEF: If It's Not One Thing It's Another
,” Circ. Heart Failure
, 6
(6
), pp. 1112
–1115
.5.
Fernandez-Golfin
, C.
, Pachon
, M.
, Corros
, C.
, Bustos
, A.
, Cabeza
, B.
, Ferreiros
, J.
, de Isla
, L. P.
, Macaya
, C.
, and Zamorano
, J.
, 2009
, “Left Ventricular Trabeculae: Quantification in Different Cardiac Diseases and Impact on Left Ventricular Morphological and Functional Parameters Assessed With Cardiac Magnetic Resonance
,” J. Cardiovasc. Med.
, 10
(11
), pp. 827
–833
.6.
van de Veerdonk
, M. C.
, Dusoswa
, S. A.
, Marcus
, J. T.
, Bogaard
, H. J.
, Spruijt
, O.
, Kind
, T.
, Westerhof
, N.
, and Vonk-Noordegraaf
, A.
, 2014
, “The Importance of Trabecular Hypertrophy in Right Ventricular Adaptation to Chronic Pressure Overload
,” Int. J. Cardiovasc. Imaging
, 30
(2
), pp. 357
–365
.7.
Halaney
, D. L.
, Sanyal
, A.
, Nafissi
, N. A.
, Escobedo
, D.
, Goros
, M.
, Michalek
, J.
, Acevedo
, P. J.
, Pérez
, W.
, Patricia Escobar
, G.
, Feldman
, M. D.
, and Han
, H.-C.
, 2017
, “The Effect of Trabeculae Carneae on Left Ventricular Diastolic Compliance: Improvement in Compliance With Trabecular Cutting
,” ASME J. Biomech. Eng.
, 139
(3
), p. 031012
.8.
Moorman
, A.
, Webb
, S.
, Brown
, N. A.
, Lamers
, W.
, and Anderson
, R. H.
, 2003
, “Development of the Heart: (1) Formation of the Cardiac Chambers and Arterial Trunks
,” Heart
, 89
(7
), pp. 806
–814
.9.
Captur
, G.
, Wilson
, R.
, Bennett
, M. F.
, Luxan
, G.
, Nasis
, A.
, de la Pompa
, J. L.
, Moon
, J. C.
, and Mohun
, T. J.
, 2016
, “Morphogenesis of Myocardial Trabeculae in the Mouse Embryo
,” J. Anat.
, 229
(2
), pp. 314
–325
.10.
Bartram
, U.
, Bauer
, J.
, and Schranz
, D.
, 2007
, “Primary Noncompaction of the Ventricular Myocardium From the Morphogenetic Standpoint
,” Pediatr. Cardiol.
, 28
(5
), pp. 325
–332
.11.
Janik
, M.
, Cham
, M. D.
, Ross
, M. I.
, Wang
, Y.
, Codella
, N.
, Min
, J. K.
, Prince
, M. R.
, Manoushagian
, S.
, Okin
, P. M.
, Devereux
, R. B.
, and Weinsaft
, J. W.
, 2008
, “Effects of Papillary Muscles and Trabeculae on Left Ventricular Quantification: Increased Impact of Methodological Variability in Patients With Left Ventricular Hypertrophy
,” J. Hypertens.
, 26
(8
), pp. 1677
–1685
.12.
Jacquier
, A.
, Thuny
, F.
, Jop
, B.
, Giorgi
, R.
, Cohen
, F.
, Gaubert
, J. Y.
, Vidal
, V.
, Bartoli
, J. M.
, Habib
, G.
, and Moulin
, G.
, 2010
, “Measurement of Trabeculated Left Ventricular Mass Using Cardiac Magnetic Resonance Imaging in the Diagnosis of Left Ventricular Non-Compaction
,” Eur. Heart J.
, 31
(9
), pp. 1098
–1104
.13.
Lin
, L. Y.
, Su
, M. Y.
, Pham
, V. T.
, Tran
, T. T.
, Wang
, Y. H.
, Tseng
, W. Y.
, Lo
, M. T.
, and Lin
, J. L.
, 2016
, “Endocardial Remodeling in Heart Failure Patients With Impaired and Preserved Left Ventricular Systolic Function—A Magnetic Resonance Image Study
,” Sci. Rep.
, 6
, p. 20868
.14.
Gati
, S.
, Chandra
, N.
, Bennett
, R. L.
, Reed
, M.
, Kervio
, G.
, Panoulas
, V. F.
, Ghani
, S.
, Sheikh
, N.
, Zaidi
, A.
, Wilson
, M.
, Papadakis
, M.
, Carre
, F.
, and Sharma
, S.
, 2013
, “Increased Left Ventricular Trabeculation in Highly Trained Athletes: Do We Need More Stringent Criteria for the Diagnosis of Left Ventricular Non-Compaction in Athletes?
,” Heart
, 99
(6
), pp. 401
–408
.15.
Gati
, S.
, Papadakis
, M.
, Papamichael
, N. D.
, Zaidi
, A.
, Sheikh
, N.
, Reed
, M.
, Sharma
, R.
, Thilaganathan
, B.
, and Sharma
, S.
, 2014
, “Reversible de Novo Left Ventricular Trabeculations in Pregnant Women: Implications for the Diagnosis of Left Ventricular Noncompaction in Low-Risk Populations
,” Circulation
, 130
(6
), pp. 475
–483
.16.
Demer
, L. L.
, and Yin
, F. C.
, 1983
, “Passive Biaxial Mechanical Properties of Isolated Canine Myocardium
,” J. Physiol.
, 339
(1
), pp. 615
–630
.17.
Sacks
, M. S.
, and Chuong
, C. J.
, 1993
, “Biaxial Mechanical Properties of Passive Right Ventricular Free Wall Myocardium
,” ASME J. Biomech. Eng.
, 115
(2
), pp. 202
–205
.18.
Kang
, T.
, Humphrey
, J. D.
, and Yin
, F. C.
, 1996
, “Comparison of Biaxial Mechanical Properties of Excised Endocardium and Epicardium
,” Am. J. Physiol.: Heart Circ. Physiol.
, 270
(6
), pp. H2169
–H2176
.19.
Javani
, S.
, Gordon
, M.
, and Azadani
, A. N.
, 2016
, “Biomechanical Properties and Microstructure of Heart Chambers: A Paired Comparison Study in an Ovine Model
,” Ann. Biomed. Eng.
, 44
(11
), pp. 3266
–3283
.20.
Okamoto
, R. J.
, Moulton
, M. J.
, Peterson
, S. J.
, Li
, D.
, Pasque
, M. K.
, and Guccione
, J. M.
, 2000
, “Epicardial Suction: A New Approach to Mechanical Testing of the Passive Ventricular Wall
,” ASME J. Biomech. Eng.
, 122
(5
), pp. 479
–487
.21.
Wang
, B.
, Tedder
, M. E.
, Perez
, C. E.
, Wang
, G.
, de Jongh Curry
, A. L.
, To
, F.
, Elder
, S. H.
, Williams
, L. N.
, Simionescu
, D. T.
, and Liao
, J.
, 2012
, “Structural and Biomechanical Characterizations of Porcine Myocardial Extracellular Matrix
,” J. Mater. Sci. Mater. Med.
, 23
(8
), pp. 1835
–1847
.22.
Han
, J. C.
, Taberner
, A. J.
, Kirton
, R. S.
, Nielsen
, P. M.
, Archer
, R.
, Kim
, N.
, and Loiselle
, D. S.
, 2011
, “Radius-Dependent Decline of Performance in Isolated Cardiac Muscle Does Not Reflect Inadequacy of Diffusive Oxygen Supply
,” Am. J. Physiol.: Heart Circ. Physiol.
, 300
(4
), pp. H1222
–H1236
.23.
Haizlip
, K. M.
, Bupha-Intr
, T.
, Biesiadecki
, B. J.
, and Janssen
, P. M.
, 2012
, “Effects of Increased Preload on the Force-Frequency Response and Contractile Kinetics in Early Stages of Cardiac Muscle Hypertrophy
,” Am. J. Physiol.: Heart Circ. Physiol.
, 302
(12
), pp. H2509
–H2517
.24.
Yin
, F. C.
, Spurgeon
, H. A.
, Weisfeldt
, M. L.
, and Lakatta
, E. G.
, 1980
, “Mechanical Properties of Myocardium From Hypertrophied Rat Hearts. A Comparison Between Hypertrophy Induced By Senescence and By Aortic Banding
,” Circ. Res.
, 46
(2
), pp. 292
–300
.25.
Pinto
, J. G.
, and Fung
, Y. C.
, 1973
, “Mechanical Properties of the Heart Muscle in the Passive State
,” J. Biomech.
, 6
(6
), pp. 597
–616
.26.
Han
, J. C.
, Taberner
, A. J.
, Nielsen
, P. M.
, and Loiselle
, D. S.
, 2013
, “Interventricular Comparison of the Energetics of Contraction of Trabeculae Carneae Isolated From the Rat Heart
,” J. Physiol.
, 591
(3
), pp. 701
–717
.27.
Weisfeldt
, M. L.
, Loeven
, W. A.
, and Shock
, N. W.
, 1971
, “Resting and Active Mechanical Properties of Trabeculae Carneae From Aged Male Rats
,” Am. J. Physiol.
, 220
(6
), pp. 1921
–1927
.28.
Feldman
, M. D.
, Copelas
, L.
, Gwathmey
, J. K.
, Phillips
, P.
, Warren
, S. E.
, Schoen
, F. J.
, Grossman
, W.
, and Morgan
, J. P.
, 1987
, “Deficient Production of Cyclic AMP: Pharmacologic Evidence of an Important Cause of Contractile Dysfunction in Patients With End-Stage Heart Failure
,” Circulation
, 75
(2
), pp. 331
–339
.29.
Gruver
, E. J.
, Morgan
, J. P.
, Stambler
, B. S.
, and Gwathmey
, J. K.
, 1994
, “Uniformity of Calcium Channel Number and Isometric Contraction in Human Right and Left Ventricular Myocardium
,” Basic Res. Cardiol.
, 89
(2
), pp. 139
–148
.30.
Appell
, H. J.
, and Stang-Voss
, C.
, 1980
, “A Peculiar Fibrillar Pattern in the Myocardial Cells of Trabeculae Carneae in the Right Ventricle of the Rat, Mouse, and Rabbit
,” Cell Tissue Res.
, 208
(1
), pp. 165
–168
.31.
Sands
, G.
, Goo
, S.
, Gerneke
, D.
, LeGrice
, I.
, and Loiselle
, D.
, 2011
, “The Collagenous Microstructure of Cardiac Ventricular Trabeculae Carneae
,” J. Struct. Biol.
, 173
(1
), pp. 110
–116
.32.
Sommer
, G.
, Schriefl
, A. J.
, Andra
, M.
, Sacherer
, M.
, Viertler
, C.
, Wolinski
, H.
, and Holzapfel
, G. A.
, 2015
, “Biomechanical Properties and Microstructure of Human Ventricular Myocardium
,” Acta Biomater.
, 24
, pp. 172
–192
.33.
Voorhees
, A. P.
, DeLeon-Pennell
, K. Y.
, Ma
, Y.
, Halade
, G. V.
, Yabluchanskiy
, A.
, Iyer
, R. P.
, Flynn
, E.
, Cates
, C. A.
, Lindsey
, M. L.
, and Han
, H. C.
, 2015
, “Building a Better Infarct: Modulation of Collagen Cross-Linking to Increase Infarct Stiffness and Reduce Left Ventricular Dilation Post-Myocardial Infarction
,” J. Mol. Cell. Cardiol.
, 85
, pp. 229
–239
.34.
Grimes
, K. M.
, Voorhees
, A.
, Chiao
, Y. A.
, Han
, H. C.
, Lindsey
, M. L.
, and Buffenstein
, R.
, 2014
, “Cardiac Function of the Naked Mole-Rat: Ecophysiological Responses to Working Underground
,” Am. J. Physiol.: Heart Circ. Physiol.
, 306
(5
), pp. H730
–H737
.35.
Eilaghi
, A.
, Flanagan
, J. G.
, Brodland
, G. W.
, and Ethier
, C. R.
, 2009
, “Strain Uniformity in Biaxial Specimens is Highly Sensitive to Attachment Details
,” ASME J. Biomech. Eng.
, 131
(9
), p. 091003
.36.
Fomovsky
, G. M.
, and Holmes
, J. W.
, 2010
, “Evolution of Scar Structure, Mechanics, and Ventricular Function After Myocardial Infarction in the Rat
,” Am. J. Physiol.: Heart Circ. Physiol.
, 298
(1
), pp. H221
–H228
.37.
Kirton
, R. S.
, Taberner
, A. J.
, Nielsen
, P. M.
, Young
, A. A.
, and Loiselle
, D. S.
, 2005
, “Effects of BDM, [Ca2+]o, and Temperature on the Dynamic Stiffness of Quiescent Cardiac Trabeculae From Rat
,” Am. J. Physiol.: Heart Circ. Physiol.
, 288
(4
), pp. H1662
–H1667
.38.
Fereidoonnezhad
, B.
, Naghdabadi
, R.
, and Holzapfel
, G. A.
, 2016
, “Stress Softening and Permanent Deformation in Human Aortas: Continuum and Computational Modeling With Application to Arterial Clamping
,” J. Mech. Behav. Biomed. Mater.
, 61
, pp. 600
–616
.39.
Urheim
, S.
, Edvardsen
, T.
, Torp
, H.
, Angelsen
, B.
, and Smiseth
, O. A.
, 2000
, “Myocardial Strain by Doppler Echocardiography: Validation of a New Method to Quantify Regional Myocardial Function
,” Circulation
, 102
(10
), pp. 1158
–1164
.40.
Halaney
, D. L.
, Acevedo
, P. J.
, Pérez
, W.
, Sanyal
, A.
, Han
, H.-C.
, and Feldman
, M.
, 2015
, “The Importance of Trabeculae Carneae for Left Ventricular Diastolic Compliance: Improvement in Compliance With Trabecular Cutting
,” J. Am. Coll. Cardiol.
, 65
(Suppl. 10
), p. A968.41.
Sommer
, G.
, Haspinger
, D.
, Andra
, M.
, Sacherer
, M.
, Viertler
, C.
, Regitnig
, P.
, and Holzapfel
, G. A.
, 2015
, “Quantification of Shear Deformations and Corresponding Stresses in the Biaxially Tested Human Myocardium
,” Ann. Biomed. Eng.
, 43
(10
), pp. 2334
–2348
.42.
Kindberg
, K.
, Haraldsson
, H.
, Sigfridsson
, A.
, Engvall
, J.
, Ingels
, N. B.
, Jr., Ebbers
, T.
, and Karlsson
, M.
, 2012
, “Myocardial Strains From 3D Displacement Encoded Magnetic Resonance Imaging
,” BMC Med. Imaging
, 12
, p. 9
.43.
Kovalova
, S.
, Necas
, J.
, and Vespalec
, J.
, 2006
, “What is a ‘Normal’ Right Ventricle?
,” Eur. J. Echocardiography
, 7
(4
), pp. 293
–297
.44.
Holzapfel
, G. A.
, and Ogden
, R. W.
, 2009
, “Constitutive Modelling of Passive Myocardium: A Structurally Based Framework for Material Characterization
,” Philos. Trans. R. Soc. A Math. Phys. Eng. Sci.
, 367
(1902
), pp. 3445
–3475
.45.
Holzapfel
, G.
, and Fereidoonnezhad
, B.
, 2017
, “Modeling of Damage in Soft Biological Tissues
,” Biomechanics of Living Organs
, Y. Payan and J. Ohayon, eds., Academic Press
, Oxford, UK
, Chap. 5.46.
Voorhees
, A. P.
, and Han
, H. C.
, 2015
, “Biomechanics of Cardiac Function
,” Compr. Physiol.
, 5
(4
), pp. 1623
–1644
.47.
Fatemifar
, F.
, and Han
, H.-C.
, 2016
, “Effect of Axial Stretch on Lumen Collapse of Arteries
,” ASME J. Biomech. Eng.
, 138
(12
), p. 124503
.48.
Wang
, C.
, Garcia
, M.
, Lu
, X.
, Lanir
, Y.
, and Kassab
, G. S.
, 2006
, “Three-Dimensional Mechanical Properties of Porcine Coronary Arteries: A Validated Two-Layer Model
,” Am. J. Physiol.: Heart Circ. Physiol.
, 291
(3
), pp. H1200
–H1209
.49.
Lin
, J.
, Lopez
, E. F.
, Jin
, Y.
, Van Remmen
, H.
, Bauch
, T.
, Han
, H. C.
, and Lindsey
, M. L.
, 2008
, “Age-Related Cardiac Muscle Sarcopenia: Combining Experimental and Mathematical Modeling to Identify Mechanisms
,” Exp. Gerontol.
, 43
(4
), pp. 296
–306
.50.
Zuo
, K.
, Pham
, T.
, Li
, K.
, Martin
, C.
, He
, Z.
, and Sun
, W.
, 2016
, “Characterization of Biomechanical Properties of Aged Human and Ovine Mitral Valve Chordae Tendineae
,” J. Mech. Behav. Biomed. Mater.
, 62
, pp. 607
–618
.51.
Pham
, T.
, and Sun
, W.
, 2014
, “Material Properties of Aged Human Mitral Valve Leaflets
,” J. Biomed. Mater. Res. Part A
, 102
(8
), pp. 2692
–2703
.52.
Azadani
, A. N.
, Chitsaz
, S.
, Matthews
, P. B.
, Jaussaud
, N.
, Leung
, J.
, Wisneski
, A.
, Ge
, L.
, and Tseng
, E. E.
, 2012
, “Biomechanical Comparison of Human Pulmonary and Aortic Roots
,” Eur. J. Cardio Thorac. Surg.
, 41
(5
), pp. 1111
–1116
.53.
Zile
, M. R.
, Baicu
, C. F.
, Ikonomidis
, J. S.
, Stroud
, R. E.
, Nietert
, P. J.
, Bradshaw
, A. D.
, Slater
, R.
, Palmer
, B. M.
, Van Buren
, P.
, Meyer
, M.
, Redfield
, M. M.
, Bull
, D. A.
, Granzier
, H. L.
, and LeWinter
, M. M.
, 2015
, “Myocardial Stiffness in Patients With Heart Failure and a Preserved Ejection Fraction: Contributions of Collagen and Titin
,” Circulation
, 131
(14
), pp. 1247
–1259
.54.
Chaturvedi
, R. R.
, Herron
, T.
, Simmons
, R.
, Shore
, D.
, Kumar
, P.
, Sethia
, B.
, Chua
, F.
, Vassiliadis
, E.
, and Kentish
, J. C.
, 2010
, “Passive Stiffness of Myocardium From Congenital Heart Disease and Implications for Diastole
,” Circulation
, 121
(8
), pp. 979
–988
.55.
Conrad
, C. H.
, Brooks
, W. W.
, Hayes
, J. A.
, Sen
, S.
, Robinson
, K. G.
, and Bing
, O. H. L.
, 1995
, “Myocardial Fibrosis and Stiffness With Hypertrophy and Heart Failure in the Spontaneously Hypertensive Rat
,” Circulation
, 91
(1
), pp. 161
–170
.56.
Pantazis
, A.
, Vischer
, A. S.
, Perez-Tome
, M. C.
, and Castelletti
, S.
, 2015
, “Diagnosis and Management of Hypertrophic Cardiomyopathy
,” Echo Res. Pract.
, 2
(1
), pp. R45
–R53
.57.
Elliott
, P. M.
, Anastasakis
, A.
, Borger
, M. A.
, Borggrefe
, M.
, Cecchi
, F.
, Charron
, P.
, Hagege
, A. A.
, Lafont
, A.
, Limongelli
, G.
, Mahrholdt
, H.
, McKenna
, W. J.
, Mogensen
, J.
, Nihoyannopoulos
, P.
, Nistri
, S.
, Pieper
, P. G.
, Pieske
, B.
, Rapezzi
, C.
, Rutten
, F. H.
, Tillmanns
, C.
, and Watkins
, H.
, 2014
, “2014 ESC Guidelines on Diagnosis and Management of Hypertrophic Cardiomyopathy: The Task Force for the Diagnosis and Management of Hypertrophic Cardiomyopathy of the European Society of Cardiology (ESC)
,” Eur. Heart J.
, 35
(39
), pp. 2733
–2779
.58.
Luo
, C.
, Ramachandran
, D.
, Ware
, D. L.
, Ma
, T. S.
, and Clark
, J. W.
, 2011
, “Modeling Left Ventricular Diastolic Dysfunction: Classification and Key Indicators
,” Theor. Biol. Medical Modell.
, 8
(1
), p. 14
.59.
Zuin
, M.
, Rigatelli
, G.
, Faggian
, G.
, and Roncon
, L.
, 2016
, “Mathematics and Cardiovascular Interventions Role of the Finite Element Modeling in Clinical Decision Making
,” JACC Cardiovasc. Interventions
, 9
(5
), pp. 507
–508
.60.
Walker
, L. A.
, and Buttrick
, P. M.
, 2013
, “The Right Ventricle: Biologic Insights and Response to Disease—Updated
,” Curr. Cardiol. Rev.
, 9
(1
), pp. 73
–81
.61.
Waldman
, L. K.
, Nosan
, D.
, Villarreal
, F.
, and Covell
, J. W.
, 1988
, “Relation Between Transmural Deformation and Local Myofiber Direction in Canine Left Ventricle
,” Circ. Res.
, 63
(3
), pp. 550
–562
.62.
Lakatta
, E. G.
, 2002
, “Age-Associated Cardiovascular Changes in Health: Impact on Cardiovascular Disease in Older Persons
,” Heart Failure Rev.
, 7
(1
), pp. 29
–49
.63.
Yabluchanskiy
, A.
, Ma
, Y.
, Chiao
, Y. A.
, Lopez
, E. F.
, Voorhees
, A. P.
, Toba
, H.
, Hall
, M. E.
, Han
, H.-C.
, Lindsey
, M. L.
, and Jin
, Y.-F.
, 2014
, “Cardiac Aging is Initiated by Matrix Metalloproteinase-9-Mediated Endothelial Dysfunction
,” Am. J. Physiol.: Heart Circ. Physiol.
, 306
(10
), pp. H1398
–H1407
.64.
Olivetti
, G.
, Melissari
, M.
, Capasso
, J. M.
, and Anversa
, P.
, 1991
, “Cardiomyopathy of the Aging Human Heart. Myocyte Loss and Reactive Cellular Hypertrophy
,” Circ. Res.
, 68
(6
), pp. 1560
–1568
.65.
Bishop
, S. P.
, Oparil
, S.
, Reynolds
, R. H.
, and Drummond
, J. L.
, 1979
, “Regional Myocyte Size in Normotensive and Spontaneously Hypertensive Rats
,” Hypertension
, 1
(4
), pp. 378
–383
.66.
Bhuiyan
, T.
, and Maurer
, M. S.
, 2011
, “Heart Failure With Preserved Ejection Fraction: Persistent Diagnosis, Therapeutic Enigma
,” Curr. Cardiovasc. Risk Rep.
, 5
(5
), pp. 440
–449
.67.
Voorhees
, A. P.
, and Han
, H. C.
, 2014
, “A Model to Determine the Effect of Collagen Fiber Alignment on Heart Function Post Myocardial Infarction
,” Theor. Biol. Med. Modell.
, 11
, p. 6
.68.
van Suylen
, R. J.
, van Bekkum
, E. E.
, Boersma
, H.
, de Kok
, L. B.
, Balk
, A. H.
, Bos
, E.
, and Bosman
, F. T.
, 1996
, “Collagen Content and Distribution in the Normal and Transplanted Human Heart: A Postmortem Quantitative Light Microscopic Analysis
,” Cardiovasc. Pathol. Off. J. Soc. Cardiovasc. Pathol.
, 5
(2
), pp. 61
–68
.69.
Lenkiewicz
, J. E.
, Davies
, M. J.
, and Rosen
, D.
, 1972
, “Collagen in Human Myocardium as a Function of Age
,” Cardiovasc. Res.
, 6
(5
), pp. 549
–555
.70.
Fomovsky
, G. M.
, Thomopoulos
, S.
, and Holmes
, J. W.
, 2010
, “Contribution of Extracellular Matrix to the Mechanical Properties of the Heart
,” J. Mol. Cell. Cardiol.
, 48
(3
), pp. 490
–496
.71.
Mujumdar
, V. S.
, and Tyagi
, S. C.
, 1999
, “Temporal Regulation of Extracellular Matrix Components in Transition From Compensatory Hypertrophy to Decompensatory Heart Failure
,” J. Hypertens.
, 17
(2
), pp. 261
–270
.72.
Holzaphel
, G. A.
, and Ogden
, R. W.
, 2009
, “On Planar Biaxial Tests for Anisotropic Nonlinearly Elastic Solids—A Continuum Mechanical Framework
,” Math. Mech. Solids
, 14
(5
), pp. 474
–489
.73.
Guccione
, J. M.
, Costa
, K. D.
, and McCulloch
, A. D.
, 1995
, “Finite Element Stress Analysis of Left Ventricular Mechanics in the Beating Dog Heart
,” J. Biomech.
, 28
(10
), pp. 1167
–1177
.Copyright © 2019 by ASME
You do not currently have access to this content.
