Anisotropy Properties of Tissues: A Basis for Fabrication of Biomimetic Anisotropic Scaffolds for Tissue Engineering
Source abstract
Abstract
Tissue engineering has been a subject of extensive scientific exploration in the last two decades making gradual inroads into clinical studies as well. Along with regenerative cells and growth factors, biomaterial scaffolds are integral to the development of a tissue engineered construct. It is now appreciated that scaffolds should mimic the target tissue properties intimately in order to provide a micro-environment milieu that allows the seeded cells to differentiate into the desired tissue. Even from a structural viewpoint, mismatch between scaffold and native matrix properties can cause cell necrosis through mechanisms such as stress shielding. One of the key properties of most body tissues is that they exhibit anisotropy. However, most fabrication methods generate isotropic scaffolds and require specific modifications to produce anisotropic scaffolds. In the last decade, the advent of additive manufacturing and bioprinting has provided facile tools to fabricate scaffolds with desired anisotropy. On the other hand, a biomimetic scaffold can be designed only when target tissue anisotropy is well known to the tissue engineer. This review presents an overview of the anisotropic properties of different tissues, which will be critical for developing biomimetic engineered constructs. The traditional anatomical records do not adequately present these properties from the perspective of designing tissue engineering scaffolds. Subsequently, present state-of-the art in development of anisotropic scaffolds as well as tissue constructs using different conventional and emerging fabrication techniques is discussed. It is expected that the readers will obtain a comprehensive reference on the research area by examining these two aspects juxtaposed to each other and gain key trends for fabrication of anisotropic scaffolds, plausibly with improved regenerative outcomes.
Source: openaire · Quality: candidate unverified · Source record ↗
Research context
OpenAlex topics: Bone Tissue Engineering Materials · Additive Manufacturing and 3D Printing Technologies · 3D Printing in Biomedical Research
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
References (100+)
Show source-provided references
1. Colombo F, Sampogna G, Cocozza G, Guraya S Y, Forgione A. Regenerative medicine: Clinical applications and future perspectives. Journal of Microscopy and Ultrastructure, 2017, 5, 1–8.10.1016/j.jmau.2016.05.002 ↗
2. Geris L, Papantoniou I. The third era of tissue engineering: Reversing the innovation drivers. Tissue Engineering — Part A, 2019, 25, 821–826.10.1089/ten.tea.2019.0064 ↗
3. Hoffman T, Khademhosseini A, Langer R. Chasing the paradigm: Clinical translation of 25 years of tissue engineering. Tissue Engineering — Part A, 2019, 25, 679–687.10.1089/ten.tea.2019.0032 ↗
4. Datta P, Ayan B, Ozbolat I T. Bioprinting for vascular and vascularized tissue biofabrication. Acta Biomaterialia, 2017, 51, 1–20.10.1016/j.actbio.2017.01.035 ↗
5. Barui A, Chowdhury F, Pandit A, Datta P. Rerouting mesenchymal stem cell trajectory towards epithelial lineage by engineering cellular niche. Biomaterials, 2018, 156, 28–44.10.1016/j.biomaterials.2017.11.036 ↗
6. Cunniffe G M, Díaz-Payno P J, Sheehy E J, Critchley S E, Almeida H V, Pitacco P, Carroll S F, Mahon O R, Dunne A, Levingstone T J, Moran C J, Brady R T, O’Brien F J, Brama P A J, Kelly D J. Tissue-specific extracellular matrix scaffolds for the regeneration of spatially complex musculoskeletal tissues. Biomaterials, 2019, 188, 63–73.10.1016/j.biomaterials.2018.09.044 ↗
7. Sano K, Ishida Y, Aida T. Synthesis of anisotropic hydrogels and their applications. Angewandte Chemie International Edition, 2018, 57, 2532–2543.10.1002/anie.201708196 ↗
8. Prince E, Kumacheva E. Design and applications of man-made biomimetic fibrillar hydrogels. Nature Reviews Materials, 2019, 4, 99–115.10.1038/s41578-018-0077-9 ↗
9. Yang B, O’Connell G D. Swelling of fiber-reinforced soft tissues is affected by fiber orientation, fiber stiffness, and lamella structure. Journal of the Mechanical Behavior of Biomedical Materials, 2018, 82, 320–328.10.1016/j.jmbbm.2018.03.039 ↗
10. Yang B, O’Connell G D. GAG content, fiber stiffness, and fiber angle affect swelling-based residual stress in the intact annulus fibrosus. Biomechanics and Modeling in Mechanobiology, 2019, 18, 617–630.10.1007/s10237-018-1105-9 ↗
11. Bini F, Pica A, Marinozzi A, Marinozzi F. A 3D model of the effect of tortuosity and constrictivity on the diffusion in mineralized collagen fibril. Scientific Reports, 2019, 9, 1–14.10.1038/s41598-019-39297-w ↗
12. Shi C, Cisewski S E, Bell P D, Yao H. Measurement of three-dimensional anisotropic diffusion by multiphoton fluorescence recovery after photobleaching. Annals of Biomedical Engineering, 2014, 42, 555–565.10.1007/s10439-013-0939-7 ↗
13. Li S, Abdel-Wahab A, Demirci E, Silberschmidt V V. Fracture of cortical bone tissue: Inelastic behavior of materials and structures under monotonic and cyclic loading. In: Altenbach H, Brünig M eds., Advanced Structured Materials, Springer, Cham, Switzerland, 2015, 143–170.
14. Novitskaya E, Chen P Y, Lee S, Castro-Ceseña A, Hirata G, Lubarda V A, McKittrick J. Anisotropy in the compressive mechanical properties of bovine cortical bone and the mineral and protein constituents. Acta Biomaterialia, 2011, 7, 3170–3177.10.1016/j.actbio.2011.04.025 ↗
15. Barati D, Karaman O, Moeinzadeh S, Kader S, Jabbari E. Material and regenerative properties of an osteon-mimetic cortical bone-like scaffold. Regenerative Biomaterials, 2019, 6, 89–98.10.1093/rb/rbz008 ↗
16. Tang S Y. Natural composites: The structure-function relationships of bone, cartilage, tendon/ligament, and the intervertebral disc. In: Ambrosio L ed., Biomedical Composites, 2nd ed, Woodhead Publishing, Cambridge, UK, 2017, 1–16.
17. Teichtahl A J, Wluka A E, Wijethilake P, Wang Y, Ghasem-Zadeh A, Cicuttini F M. Wolff’s law in action: A mechanism for early knee osteoarthritis. Arthritis Research and Therapy, 2015, 17, 1–9.10.1186/s13075-014-0514-0 ↗
18. Li S, Demirci E, Silberschmidt V V. Variability and anisotropy of mechanical behavior of cortical bone in tension and compression. Journal of the Mechanical Behavior of Biomedical Materials, 2013, 21, 109–120.10.1016/j.jmbbm.2013.02.021 ↗
19. Iyo T, Maki Y, Sasaki N, Nakata M. Anisotropic viscoelastic properties of cortical bone. Journal of Biomechanics, 2004, 37, 1433–1437.10.1016/j.jbiomech.2003.12.023 ↗
20. Hardisty M R, Garcia T C, Choy S, Dahmubed J, Stover S M, Fyhrie D P. Stress-whitening occurs in demineralized bone. Bone, 2013, 57, 367–374.10.1016/j.bone.2013.08.029 ↗
21. Szabó M E, Thurner P J. Anisotropy of bovine cortical bone tissue damage properties. Journal of Biomechanics, 2013, 46, 2–6.10.1016/j.jbiomech.2012.08.002 ↗
22. Faingold A, Cohen S R, Shahar R, Weiner S, Rapoport L, Wagner H D. The effect of hydration on mechanical anisotropy, topography and fibril organization of the osteonal lamellae. Journal of Biomechanics, 2014, 47, 367–372.10.1016/j.jbiomech.2013.11.022 ↗
23. Rohrbach D, Lakshmanan S, Peyrin F, Langer M, Gerisch A, Grimal Q, Laugier P, Raum K. Spatial distribution of tissue level properties in a human femoral cortical bone. Journal of Biomechanics, 2012, 45, 2264–2270.10.1016/j.jbiomech.2012.06.003 ↗
24. Casanova M, Schneider P, Müller R, Carnelli D, Balmelli A, Courty D. Nanoindentation analysis of the micromechanical anisotropy in mouse cortical bone. Royal Society Open Science, 2017, 4, 1–9.10.1098/rsos.160971 ↗
25. Cardoso L. Structure-function relationship in bone: Anisotropic mechanical properties of trabecular bone determined using poroelastic ultrasound. The Journal of the Acoustical Society of America, 2016, 140, 3080–3080.10.1121/1.4969595 ↗
26. Santiuste C, Rodríguez-Millán M, Giner E, Miguélez H. The influence of anisotropy in numerical modeling of orthogonal cutting of cortical bone. Composite Structures, 2014, 116, 423–431.10.1016/j.compstruct.2014.05.031 ↗
27. Moussa D G, Aparicio C. Present and future of tissue engineering scaffolds for dentin-pulp complex regeneration. Journal of Tissue Engineering and Regenerative Medicine, 2019, 13, 58–75.
28. Huo B. An inhomogeneous and anisotropic constitutive model of human dentin. Journal of Biomechanics, 2005, 38, 587–594.10.1016/j.jbiomech.2004.03.028 ↗
29. Shinno Y, Ishimoto T, Saito M, Uemura R, Arino M, Marumo K, Nakano T, Hayashi M. Comprehensive analyses of how tubule occlusion and advanced glycation end-products diminish strength of aged dentin. Scientific Reports, 2016, 6, 19849.10.1038/srep19849 ↗
30. Lu X, Fernández M P, Bradley R S, Rawson S D, O’Brien M, Hornberger B, Leibowitz M, Tozzi G, Withers P J. Anisotropic crack propagation and deformation in dentin observed by four-dimensional X-ray nano-computed tomography. Acta Biomaterialia, 2019, 96, 400–411.10.1016/j.actbio.2019.06.042 ↗
31. Zaytsev D, Ivashov A, Panfilov P. Anisotropy of the mechanical properties of human dentin under shear testing. Materials Letters, 2015, 138, 219–221.10.1016/j.matlet.2014.09.140 ↗
32. Muslov S A. Anisotropy of Poisson’s ratio of dentin and enamel. IOP Conference Series: Materials Science and Engineering, 2018, 441, 1–9.10.1088/1757-899X/441/1/012032 ↗
33. Lertchirakarn V, Palamara J E A, Messer H H. Anisotropy of tensile strength of root dentin. Journal of Dental Research, 2001, 80, 453–456.10.1177/00220345010800021001 ↗
34. Urbanek O, Kolbuk D, Wróbel M. Articular cartilage: New directions and barriers of scaffolds development — Review. International Journal of Polymeric Materials and Polymeric Biomaterials, 2019, 68, 396–410.10.1080/00914037.2018.1452224 ↗
35. Ratcliffe A, Fryer P R, Hardingham T E. The distribution of aggregating proteoglycans in articular cartilage: Comparison of quantitative immunoelectron microscopy with radioimmunoassay and biochemical analysis. Journal of Histochemistry & Cytochemistry, 1984, 32, 193–201.10.1177/32.2.6363519 ↗
36. Liu M, Zeng X, Ma C, Yi H, Ali Z, Mou X, Li S, Deng Y, He N. Injectable hydrogels for cartilage and bone tissue engineering. Bone Research, 2017, 5, 1–20.
37. Hardin J A, Cobelli N, Santambrogio L. Consequences of metabolic and oxidative modifications of cartilage tissue. Nature Reviews Rheumatology, 2015, 11, 521–529.10.1038/nrrheum.2015.70 ↗
38. Muir H, Bullough P, Maroudas A. The distribution of collagen in human articular cartilage with some of its physiological implications. The Journal of Bone and Joint Surgery, 1970, 52, 554–563.10.1302/0301-620X.52B3.554 ↗
39. Akizuki S, Mow V C, Müller F, Pita J C, Howell D S, Manicourt D H. Tensile properties of human knee joint cartilage: I. Influence of ionic conditions, weight bearing, and fibrillation on the tensile modulus. Journal of Orthopaedic Research, 1986, 4, 379–392.10.1002/jor.1100040401 ↗
40. Schinagl R M, Gurskis D, Chen A C, Sah R L. Depthdependent confined compression modulus of full — thickness bovine articular cartilage. Journal of Orthopaedic Research, 1997, 15, 499–506.10.1002/jor.1100150404 ↗
41. Mansfield J C, Bell J S, Winlove C P. The micromechanics of the superficial zone of articular cartilage. Osteoarthritis and Cartilage, 2015, 23, 1806–1816.10.1016/j.joca.2015.05.030 ↗
42. Maier F, Drissi H, Pierce D M. Shear deformations of human articular cartilage: Certain mechanical anisotropies apparent at large but not small shear strains. Journal of the Mechanical Behavior of Biomedical Materials, 2017, 65, 53–65.10.1016/j.jmbbm.2016.08.012 ↗
43. Xia Y, Zheng S, Szarko M, Lee J. Anisotropic properties of bovine nasal cartilage. Microscopy Research and Technique, 2012, 75, 300–306.10.1002/jemt.21058 ↗
44. Sophia Fox A J, Bedi A, Rodeo S A. The basic science of articular cartilage: Structure, composition, and function. Sports Health, 2009, 1, 461–468.10.1177/1941738109350438 ↗
45. Gastaldi D, Taffetani M, Raiteri R, Vena P. Effect of the anisotropic permeability in the frequency dependent properties of the superficial layer of articular cartilage. Computer Methods in Biomechanics and Biomedical Engineering, 2018, 21, 635–644.10.1080/10255842.2018.1504214 ↗
46. Shi C, Wright G J, Ex-lubeskie C L, Bradshaw A D, Yao H. Relationship between anisotropic diffusion properties and tissue morphology in porcine TMJ disc. Osteoarthritis and Cartilage, 2013, 21, 625–633.10.1016/j.joca.2013.01.010 ↗
47. Beaupre A, Choukroun R, Guidouin R, Garneau R, Gerardin H, Cardou A. Knee menisci. Correlation between microstructure and biomechanics. Clinical Orthopaedics and Related Research, 1986, 208, 72–75.
48. Fithian D C, Kelly M A, Mow V C. Material properties and structure-function relationships in the menisci. Clinical Orthopaedics and Related Research, 1990, 252, 19–31.10.1097/00003086-199003000-00004 ↗
49. Li Q, Qu F, Han B, Wang C, Li H, Mauck R L, Han L. Micromechanical anisotropy and heterogeneity of the meniscus extracellular matrix. Acta Biomaterialia, 2017, 54, 356–366.10.1016/j.actbio.2017.02.043 ↗
50. Hukins D W L. Biomechanical properties of collagen. Collagen in Health and Disease, Weiss J B and Jayson M I V eds., Churchill Livingstone, London, 1982, 49–72.
51. Gabrion A, Aimedieu P, Laya Z, Havet E, Mertl P, Grebe R, Laude M. Relationship between ultrastructure and biomechanical properties of the knee meniscus. Surgical and Radiologic Anatomy, 2005, 27, 507–510.10.1007/s00276-005-0031-6 ↗
52. Leslie B W, Gardner D L, McGeough J A, Moran R S. Anisotropic response of the human knee joint meniscus to unconfined compression. Proceedings of the Institution of Mechanical Engineers. Part H, Journal of Engineering in Medicine, 2000, 214, 631–635.10.1243/0954411001535651 ↗
53. Puetzer J L, Koo E, Bonassar L J. Induction of fiber alignment and mechanical anisotropy in tissue engineered menisci with mechanical anchoring. Journal of Biomechanics, 2015, 48, 1436–1443.10.1016/j.jbiomech.2015.02.033 ↗
54. Rattner J B, Matyas J R, Barclay L, Holowaychuk S, Sciore P, Lo I K Y, Shrive N G, Frank C B, Achari Y, Hart D A. New understanding of the complex structure of knee menisci: Implications for injury risk and repair potential for athletes. Scandinavian Journal of Medicine & Science in Sports, 2011, 21, 543–553.10.1111/j.1600-0838.2009.01073.x ↗
55. Petersen W, Tillmann B. Collagenous fibril texture of the human knee joint menisci. Anatomy and Embryology, 1998, 197, 317–324.10.1007/s004290050141 ↗
56. Peloquin J M, Santare M H, Elliott D M. Advances in quantification of meniscus tensile mechanics including nonlinearity, yield, and failure. Journal of Biomechanical Engineering, 2016, 138, 1–13.10.1115/1.4032354 ↗
57. Gharpuray V M. Fibrocartilage. In: Murphy W, Black J, Hastings G eds., Handbook of Biomaterial Properties, Springer, New York, 2016, 45–54.10.1007/978-1-4939-3305-1_5 ↗
58. Kleinhans K L, Jackson A R. Hydraulic permeability of meniscus fibrocartilage measured via direct permeation: Effects of tissue anisotropy, water volume content, and compressive strain. Journal of Biomechanics, 2018, 72, 215–221.10.1016/j.jbiomech.2018.03.011 ↗
59. Kleinhans K L, McMahan J B, Jackson A R. Electrical conductivity and ion diffusion in porcine meniscus: effects of strain, anisotropy, and tissue region. Journal of Biomechanics, 2016, 49, 3041–3046.10.1016/j.jbiomech.2016.06.011 ↗
60. Xu J, Liu S, Wang S, Qiu P, Chen P, Lin X, Fang X. Decellularised nucleus pulposus as a potential biologic scaffold for disc tissue engineering. Materials Science and Engineering: C, 2019, 99, 1213–1225.10.1016/j.msec.2019.02.045 ↗
61. Gao X, Zhu Q, Gu W. An anisotropic multiphysics model for intervertebral disk. Journal of Applied Mechanics, 2016, 83, 210111–210118.
62. Raj P P. Intervertebral disc: Anatomy-physiology-pathophysiology- treatment. Pain Practice, 2008, 8, 18–44.10.1111/j.1533-2500.2007.00171.x ↗
63. Fujita Y, Wagner D R, Biviji A A, Duncan N A, Lotz J C. Anisotropic shear behavior of the annulus fibrosus: Effect of harvest site and tissue prestrain. Medical Engineering and Physics, 2000, 22, 349–357.10.1016/S1350-4533(00)00053-9 ↗
64. Maquart F X, Monboisse J C. Extracellular matrix and wound healing. Pathologie Biologie, 2014, 62, 91–95.10.1016/j.patbio.2014.02.007 ↗
65. Humzah M D, Soames R W. Human intervertebral disc: Structure and function. The Anatomical Record, 1988, 220, 337–356.10.1002/ar.1092200402 ↗
66. Yang B, O’Connell G D. Effect of collagen fibre orientation on intervertebral disc torsion mechanics. Biomechanics and Modeling in Mechanobiology, 2017, 16, 2005–2015.10.1007/s10237-017-0934-2 ↗
67. Dittmar R, Van Rijsbergen M M, Ito K. Moderately degenerated human intervertebral disks exhibit a less geometrically specific collagen fiber orientation distribution. Global Spine Journal, 2016, 6, 439–446.10.1055/s-0035-1564805 ↗
68. Nerurkar N L, Elliott D M, Mauck R L. Mechanics of oriented electrospun nanofibrous scaffolds for annulus fibrosus tissue engineering. Journal of Orthopaedic Research, 2007, 25, 1018–1028.10.1002/jor.20384 ↗
69. Newell N, Little J P, Christou A, Adams M A, Adam C J, Masouros S D. Biomechanics of the human intervertebral disc: A review of testing techniques and results. Journal of the Mechanical Behavior of Biomedical Materials, 2017, 69, 420–434.10.1016/j.jmbbm.2017.01.037 ↗
70. Schmidt J L, Tweten D J, Badachhape A A, Reiter A J, Okamoto R J, Garbow J R, Bayly P V. Measurement of anisotropic mechanical properties in porcine brain white matter ex vivo using magnetic resonance elastography. Journal of the Mechanical Behavior of Biomedical Materials, 2018, 79, 30–37.10.1016/j.jmbbm.2017.11.045 ↗
71. Vadapalli R, Mulukutla R, Vadapalli A S, Vedula R R. Quantitative predictive imaging biomarkers of lumbar intervertebral disc degeneration. Asian Spine Journal, 2019, 13, 527–534.10.31616/asj.2018.0166 ↗
72. Jana S, Levengood S K L, Zhang M. Anisotropic materials for skeletal-muscle-tissue engineering. Advanced Materials, 2016, 28, 10588–10612.10.1002/adma.201600240 ↗
73. Eskandari M, Arvayo A L, Levenston M E. Mechanical properties of the airway tree: Heterogeneous and anisotropic pseudoelastic and viscoelastic tissue responses. Journal of Applied Physiology, 2018, 125, 878–888.10.1152/japplphysiol.00090.2018 ↗
74. Li L P, Herzog W. Strain-rate dependence of cartilage stiffness in unconfined compression: The role of fibril reinforcement versus tissue volume change in fluid pressurization. Journal of biomechanics, 2004, 37, 375–382.10.1016/S0021-9290(03)00263-X ↗
75. Mizrahi J, Karni Z, Polishuk W Z. Isotropy and anisotropy of uterine muscle during labor contraction. Journal of Biomechanics, 2018, 13, 211–218.10.1016/0021-9290(80)90364-4 ↗
76. Ajalloueian F, Lemon G, Hilborn J, Chronakis I S, Fossum M. Bladder biomechanics and the use of scaffolds for regenerative medicine in the urinary bladder. Nature Reviews Urology, 2018, 15, 155.10.1038/nrurol.2018.5 ↗
77. Korossis S, Bolland F, Southgate J, Ingham E, Fisher J. Regional biomechanical and histological characterisation of the passive porcine urinary bladder: Implications for augmentation and tissue engineering strategies. Biomaterials, 2009, 30, 266–275.10.1016/j.biomaterials.2008.09.034 ↗
78. Borsdorf M, Tomalka A, Stutzig N, Morales-Orcajo E, Böl M, Siebert T. Locational and directional dependencies of smooth muscle properties in pig urinary bladder. Frontiers in Physiology, 2019, 10, 63.10.3389/fphys.2019.00063 ↗
79. Morales-Orcajo E, Siebert T, Böl M. Location-dependent correlation between tissue structure and the mechanical behaviour of the urinary bladder. Acta Biomaterialia, 2018, 75, 263–278.10.1016/j.actbio.2018.05.014 ↗
80. Fine M L, King T L, Ali H, Sidker N, Cameron T M. Wall structure and material properties cause viscous damping of swimbladder sounds in the oyster toadfish Opsanus tau. Proceedings of the Royal Society B: Biological Sciences, 2016, 283, 1–9.10.1098/rspb.2016.1094 ↗
81. Sacks M S, Gloeckner D C. Quantification of the fiber architecture and biaxial mechanical behavior of porcine intestinal submucosa. Journal of Biomedical Materials Research, 1999, 46, 1–10.10.1002/(SICI)1097-4636(199907)46:1<1::AID-JBM1>3.0.CO;2-7 ↗
82. Kwon H, Guasch M, Nagy J A, Rutkove S B, Sanchez B. New electrical impedance methods for the in situ measurement of the complex permittivity of anisotropic skeletal muscle using multipolar needles. Scientific Reports, 2019, 9, 1–16.10.1038/s41598-018-37186-2 ↗
83. Liu D, Yan G. A Multi-layer finite element model based on anisotropic hyperelastic fiber reinforcements within intestinal walls. Nano Biomedicine and Engineering, 2017, 9, 291–297.10.5101/nbe.v9i4.p291-297 ↗
84. Patel D J, Janicki J S, Carew T E. Static anisotropic elastic properties of the aorta in living dogs. Circulation Research, 1969, 25, 765–799.10.1161/01.RES.25.6.765 ↗
85. Kas’yanov V A, Purinya B A, Tseders É É. Determination of the shear modulus of human blood-vessel walls. Polymer Mechanics, 1978, 14, 753–755.
86. Kohn J C, Lampi M C, Reinhart-King C A. Age-related vascular stiffening: Causes and consequences. Frontiers in Genetics, 2015, 6, 1–17.10.3389/fgene.2015.00112 ↗
87. Holzapfel G A. Determination of material models for arterial walls from uniaxial extension tests and histological structure. Journal of Theoretical Biology, 2006, 238, 290–302.10.1016/j.jtbi.2005.05.006 ↗
88. Muiznieks L D, Keeley F W. Molecular assembly and mechanical properties of the extracellular matrix: A fibrous protein perspective. Biochimica et Biophysica Acta - Molecular Basis of Disease, 2013, 1832, 866–875.10.1016/j.bbadis.2012.11.022 ↗
89. Wang Y, Hahn J, Zhang Y. Mechanical properties of arterial elastin with water loss. Journal of Biomechanical Engineering, 2018, 140, 41012–41018.10.1115/1.4038887 ↗
90. Qi N, Gao H, Ogden R W, Hill N A, Holzapfel G A, Han H-C, Luo X. Investigation of the optimal collagen fibre orientation in human iliac arteries. Journal of the Mechanical Behavior of Biomedical Materials, 2015, 52, 108–119.10.1016/j.jmbbm.2015.06.011 ↗
91. Zou Y, Zhang Y. An experimental and theoretical study on the anisotropy of elastin network. Annals of Biomedical Engineering, 2009, 37, 1572–1583.10.1007/s10439-009-9724-z ↗
92. Sato M, Niimi H, Okumura A, Handa H, Hayashi K, Moritake K. Axial mechanical properties of arterial walls and their anisotropy. Medical and Biological Engineering and Computing, 1979, 17, 170–176.10.1007/BF02440925 ↗
93. Agrawal V, Kollimada S A, Byju A G, Gundiah N. Regional variations in the nonlinearity and anisotropy of bovine aortic elastin. Biomechanics and Modeling in Mechanobiology, 2013, 12, 1181–1194.10.1007/s10237-013-0474-3 ↗
94. Yu X, Wang Y, Zhang Y. Transmural variation in elastin fiber orientation distribution in the arterial wall. Journal of the Mechanical Behavior of Biomedical Materials, 2018, 77, 745–753.10.1016/j.jmbbm.2017.08.002 ↗
95. Hammer P E, Pacak C A, Howe R D, del Nido P J. Collagen bundle orientation explains aortic valve leaflet coaptation. In: Ourselin S, Rueckert D, Smith N eds., Functional Imaging and Modeling of the Heart, Springer, Berlin Heidelberg, Germany, 2013, 409–415.10.1007/978-3-642-38899-6_48 ↗
96. Auricchio F, Conti M, Morganti S. Aortic biological prosthetic valve for open-surgery and percutaneous implant: Procedure simulation and performance assessment. In: Franz T ed., Cardiovascular and Cardiac Therapeutic Devices, Springer, Berlin Heidelberg, Germany, 2014, 131–168.
97. Hasan A, Ragaert K, Swieszkowski W, Selimovic Š, Paul A, Camci-Unal G, Mofrad M R K, Khademhosseini A. Biomechanical properties of native and tissue engineered heart valve constructs. Journal of Biomechanics, 2014, 47, 1949–1963.10.1016/j.jbiomech.2013.09.023 ↗
98. Vesely I, Noseworthy R. Micromechanics of the fibrosa and the ventricularis in aortic valve leaflets. Journal of Biomechanics, 2018, 25, 111–113.
99. Lo D, Vesely I. Biaxial strain analysis of the porcine aortic valve. The Annals of Thoracic Surgery, 2018, 60, 374–378.10.1016/0003-4975(95)00249-K ↗
100. Pham T, Sun W. Material properties of aged human mitral valve leaflets. Journal of Biomedical Materials Research Part A, 2014, 102, 2692–2703.10.1002/jbm.a.34939 ↗