Living tissues show an adaptive response to mechanical loading by changing their internal structure and morphology. Understanding this response is essential for successful tissue engineering of load-bearing structures, such as the aortic valve. In this study, mechanically induced remodeling of the collagen architecture in the aortic valve was investigated. It was hypothesized that, in uniaxially loaded regions, the fibers aligned with the tensile principal stretch direction. For biaxial loading conditions, on the other hand, it was assumed that the collagen fibers aligned with directions situated between the principal stretch directions. This hypothesis has already been applied successfully to study collagen remodeling in arteries. The predicted fiber architecture represented a branching network and resembled the macroscopically visible collagen bundles in the native leaflet. In addition, the complex biaxial mechanical behavior of the native valve could be simulated qualitatively with the predicted fiber directions. The results of the present model might be used to gain further insight into the response of tissue engineered constructs during mechanical conditioning.
1.
Sodian
, R.
, Hoerstrup
, S. P.
, Sperling
, J. S.
, Daebritz
, S.
, Martin
, D. P.
, Moran
, A. M.
, Kim
, B. S.
, Schoen
, F. J.
, Vacanti
, J. P.
, and Mayer
, J. E.
, Jr, 2000, “Early in vivo experience with tissue engineered trileaflet heart valves
,” Circulation
0009-7322, 102
(19
), pp. III22
–III29
.2.
Hoerstrup
, S. P.
, Sodian
, R.
, Daebritz
, S.
, Wang
, J.
, Bacha
, E. A.
, Martin
, D. P.
, Moran
, A. M.
, Guleserian
, K. J.
, Sperling
, J. S.
, Kaushal
, S.
, Vacanti
, J. P.
, Schoen
, F. J.
, and Mayer
, J. E.
, Jr, 2000, “Functional living trileaflet heart valves grown in vitro
,” Circulation
0009-7322, 102
(19
), pp. III44
–III49
.3.
Sodian
, R.
, Hoerstrup
, S. P.
, Sperling
, J. S.
, Daebritz
, S.
, Martin
, D. P.
, Schoen
, F. J.
, Vacanti
, J. P.
, and Mayer
, J. E.
, Jr, 2000, “Tissue engineering of heart valves: in vitro experiences
,” Ann. Thorac. Surg.
0003-4975, 70
(1
), pp. 140
–144
.4.
Billiar
, K. L.
, and Sacks
, M. S.
, 2000, “Biaxial mechanical properties of the natural and glutaraldehyde treated aortic valve cusp—Part I: Experimental results
,” ASME J. Biomech. Eng.
0148-0731, 122
(1
), pp. 23
–30
.5.
Billiar
, K. L.
, and Sacks
, M. S.
, 2000, “Biaxial mechanical properties of the natural and glutaraldehyde treated aortic valve cusp—Part II: A structural constitutive model
,” ASME J. Biomech. Eng.
0148-0731, 122
(4
), pp. 327
–335
.6.
Guidry
, C.
, and Grinnell
, F.
, 1985, “Studies on the mechanism of hydrated collagen gel reorganization by human skin fibroblasts
,” J. Cell. Sci.
0021-9533, 79
, pp. 67
–81
.7.
Birk
, D. E.
, and Trelstad
, R. L.
, 1984, “Extracellular compartments in matrix morphogenesis: Collagen fibril, bundle, and lamellar formation by corneal fibroblasts
,” J. Cell Biol.
0021-9525, 99
(6
), pp. 2024
–2033
.8.
Sawhney
, R. K.
, and Howard
, J.
, 2002, “Slow local movements of collagen fibers by fibroblasts drive the rapid global self-organization of collagen gels
,” J. Cell Biol.
0021-9525, 157
(6
), pp. 1083
–1091
.9.
Bishop
, J. E.
, and Lindahl
, G.
, 1999, “Regulation of cardiovascular collagen synthesis by mechanical load
,” Cardiovasc. Res.
0008-6363, 42
(1
), pp. 27
–44
.10.
MacKenna
, D.
, Summerour
, S. R.
, and Villarreal
, F. J.
, 2000, “Role of mechanical factors in modulating cardiac fibroblast function and extracellular matrix synthesis
,” Cardiovasc. Res.
0008-6363, 46
(2
), pp. 257
–263
.11.
Prajapati
, R. T.
, Chavally-Mis
, B.
, Herbage
, D.
, Eastwood
, M.
, and Brown
, R. A.
, 2000, “Mechanical loading regulates protease production by fibroblasts in three-dimensional collagen substrates
,” Wound Repair Regen
1067-1927, 8
(3
), pp. 226
–237
.12.
Rubin
E.
, and Farber
, J. L.
, 1998, Pathology
, Lippincott-Raven
, Philadelphia.13.
Boerboom
, R. A.
, Driessen
, N. J. B.
, Bouten
, C. V. C.
, Huyghe
, J. M.
, and Baaijens
, F. P. T.
, 2003, “A finite element model of mechanically induced collagen fiber synthesis and degradation in the aortic valve
,” Ann. Biomed. Eng.
0090-6964, 31
(9
), pp. 1040
–1053
.14.
Driessen
, N. J. B.
, Boerboom
, R. A.
, Huyghe
, J. M.
, Bouten
, C. V. C.
, and Baaijens
, F. P. T.
, 2003, “Computational analyses of mechanically induced collagen fiber remodeling in the aortic heart valve
,” ASME J. Biomech. Eng.
0148-0731, 125
(4
), pp. 549
–557
.15.
Driessen
, N. J. B.
, Peters
, G. W. M.
, Huyghe
, J. M.
, Bouten
, C. V. C.
, and Baaijens
, F. P. T.
, 2003, “Remodelling of continuously distributed collagen fibres in soft connective tissues
,” J. Biomech.
0021-9290, 36
(8
), pp. 1151
–1158
.16.
Sacks
, M. S.
, Smith
, D. B.
, and Hiester
, E. D.
, 1997, “A small angle light scattering device for planar connective tissue microstructural analysis
,” Ann. Biomed. Eng.
0090-6964, 25
(4
), pp. 678
–689
.17.
Rhodin
, J. A. G.
, 1980, “Architecture of the vessel wall
,” in Handbook of Physiology, The Cardiovascular System
, H. V.
, Sparks
, Jr., D. F.
, Bohr
, A. D.
Somlyo
, and S. R.
Geiger
, eds., American Physiological Society
, Bethesda, Maryland, Vol. 2
, pp. 1
–31
.18.
Driessen
, N. J. B.
, Wilson
, W.
, Bouten
, C. V. C.
, and Baaijens
, F. P. T.
, 2004, “A computational model for collagen fibre remodelling in the arterial wall
,” J. Theor. Biol.
0022-5193, 226
(1
), pp. 53
–64
.19.
Finlay
, H. M.
, McCullough
, L.
, and Canham
, P. B.
, 1995, “Three-dimensional collagen organization of human brain arteries at different transmural pressures
,” J. Vasc. Res.
1018-1172, 32
(5
), pp. 301
–312
.20.
Holzapfel
, G. A.
, Gasser
, T. C.
, and Stadler
, M.
, 2002, “A structural model for the viscoelastic behavior of arterial walls: Continuum formulation and finite element analysis
,” Eur. J. Mech. A/Solids
0997-7538, 21
(3
), pp. 441
–463
.21.
van Oijen
, C. H. G. A.
, 2003, “Mechanics and design of fiber-reinforced vascular prostheses
,” Ph.D. thesis, Technische Universiteit Eindhoven.22.
Bathe
, K. J.
, 1996, Finite Element Procedures
, Prentice Hall
, Englewood Cliffs, NJ.23.
Segal
, A.
, 1984, SEPRAN User Manual, Standard Problems and Programmers Guide
, Ingenieursbureau SEPRA
, Leidschendam, the Netherlands.24.
Thubrikar
, M. J.
, Aouad
, J.
, and Nolan
, S. P.
, 1986, “Comparison of the in vivo and in vitro mechanical properties of aortic valve leaflets
,” J. Thorac. Cardiovasc. Surg.
0022-5223, 92
(1
), pp. 29
–36
.25.
Mol
, A.
, Bouten
, C. V.
, Zund
, G.
, Gunter
, C. I.
, Visjager
, J. F.
, Turina
, M. I.
, Baaijens
, F. P.
, and Hoerstrup
, S. P.
, 2003, “The relevance of large strains in functional tissue engineering of heart valves
,” Thorac. Cardiovasc. Surg.
0171-6425, 51
(2
), pp. 78
–83
.26.
Sauren
, A. A. H. J.
, 1981, “The mechanical behaviour of the aortic valve
,” Ph.D. thesis, Technische Hogeschool, Eindhoven.27.
Sacks
, M. S.
, Smith
, D. B.
, and Hiester
, E. D.
, 1998, “The aortic valve microstructure: effects of transvalvular pressure
,” J. Biomed. Mater. Res.
0021-9304, 41
(1
), pp. 131
–141
.28.
Orberg
, J. W.
, Klein
, L.
, and Hiltner
, A.
, 1982, “Scanning electron microscopy of collagen fibers in intestine
,” Connect. Tissue Res.
0300-8207, 9
(3
), pp. 187
–193
.29.
Sacks
, M. S.
, and Gloeckner
, D. C.
, 1999, “Quantification of the fiber architecture and biaxial mechanical behavior of porcine intestinal submucosa
,” J. Biomed. Mater. Res.
0021-9304, 46
(1
), pp. 1
–10
.30.
Gloeckner
, D. C.
, Sacks
, M. S.
, Billiar
, K. L.
, and Bachrach
, N.
, 2000, “Mechanical evaluation and design of a multilayered collagenous repair biomaterial
,” J. Biomed. Mater. Res.
0021-9304, 52
(2
), pp. 365
–373
.31.
Sacks
, M. S.
, and Chuong
, C. J.
, 1992, “Characterization of collagen fiber architecture in the canine diaphragmatic central tendon
,” ASME J. Biomech. Eng.
0148-0731, 114
(2
), pp. 183
–190
.32.
Barocas
, V. H.
, and Tranquillo
, R. T.
, 1997, “An anisotropic biphasic theory of tissue-equivalent mechanics: the interplay among cell traction, fibrillar network deformation, fibril alignment and cell contact guidance
,” ASME J. Biomech. Eng.
0148-0731, 119
(2
), pp. 137
–145
.33.
Barocas
, V. H.
, and Tranquillo
, R. T.
, 1997, “A finite element solution for the anisotropic biphasic theory of tissue-equivalent mechanics: the effect of contact guidance on isometric cell traction measurement
,” ASME J. Biomech. Eng.
0148-0731, 119
(3
), pp. 261
–268
.34.
Sacks
, M. S.
, 2003, “Incorporation of experimentally-derived fiber orientation into a structural constitutive model for planar collagenous tissues
,” ASME J. Biomech. Eng.
0148-0731, 125
(2
), pp. 280
–287
.35.
Lanir
, Y.
, 1983, “Constitutive equations for fibrous connective tissues
,” J. Biomech.
0021-9290, 16
(1
), pp. 1
–12
.36.
Nakatsuji
, N.
, and Johnson
, K. E.
, 1984, “Experimental manipulation of a contact guidance system in amphibian gastrulation by mechanical tension
,” Nature (London)
0028-0836, 307
(5950
), pp. 453
–455
.37.
Rijcken
, J.
, Bovendeerd
, P. H.
, Schoofs
, A. J.
, van Campen
, D. H.
, and Arts
, T.
, 1997, “Optimization of cardiac fiber orientation for homogeneous fiber strain at beginning of ejection
,” J. Biomech.
0021-9290, 30
(10
), pp. 1041
–1049
.38.
Rijcken
, J.
, Bovendeerd
, P. H.
, Schoofs
, A. J.
, van Campen
, D. H.
, and Arts
, T.
, 1999, “Optimization of cardiac fiber orientation for homogeneous fiber strain during ejection
,” Ann. Biomed. Eng.
0090-6964, 27
(3
), pp. 289
–297
.39.
Taber
, L. A.
, 1998, “A model for aortic growth based on fluid shear and fiber stresses
,” J. Biomech. Eng.
0148-0731, 120
(3
), pp. 348
–354
.40.
Huang
, C.
, and Yannas
, I. V.
, 1977, “Mechanochemical studies of enzymatic degradation of insoluble collagen fibers
,” J. Biomed. Mater. Res.
0021-9304, 11
(1
), pp. 137
–154
.41.
Niklason
, L. E.
, Gao
, J.
, Abbott
, W. M.
, Hirschi
, K. K.
, Houser
, S.
, Marini
, R.
, and Langer
, R.
, 1999, “Functional arteries grown in vitro
,” Science
0036-8075, 284
(5413
), pp. 489
–493
.42.
Kim
, B. S.
, Nikolovski
, J.
, Bonadio
, J.
, and Mooney
, D. J.
, 1999, “Cyclic mechanical strain regulates the development of engineered smooth muscle tissue
,” Nat. Biotechnol.
1087-0156, 17
(10
), pp. 979
–983
.43.
Prabhakar
, V.
, Grinstaff
, M. W.
, Alarcon
, J.
, Knors
, C.
, Solan
, A. K.
, and Niklason
, L. E.
, 2003, “Engineering porcine arteries: effects of scaffold modification
,” J. Biomed. Mater. Res.
0021-9304, 67A
(1
), pp. 303
–311
.44.
Kolpakov
, V.
, Rekhter
, M. D.
, Gordon
, D.
, Wang
, W. H.
, and Kulik
, T. J.
, 1995, “Effect of mechanical forces on growth and matrix protein synthesis in the in vitro pulmonary artery. Analysis of the role of individual cell types
,” Circ. Res.
0009-7330, 77
(4
), pp. 823
–831
.45.
Carver
, W.
, Nagpal
, M. L.
, Nachtigal
, M.
, Borg
, T. K.
, and Terracio
, L.
, 1991, “Collagen expression in mechanically stimulated cardiac fibroblasts
,” Circ. Res.
0009-7330, 69
(1
), pp. 116
–122
.46.
Doillon
, C. J.
, Dunn
, M. G.
, Bender
, E.
and Silver
, F. H.
, 1985, “Collagen fiber formation in repair tissue: development of strength and toughness
,” Coll. Relat. Res.
0174-173X, 5
(6
), pp. 481
–492
.47.
Silver
, F. H.
, Freeman
, J. W.
, and Seehra
, G. P.
, 2003, “Collagen self-assembly and the development of tendon mechanical properties
,” J. Biomech.
0021-9290, 36
(10
), pp. 1529
–1553
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