Hollow tubular tissues and organs of our body have various functions: gastrointestinal (esophagus), respiratory (trachea), and vascular (veins, arteries). A panel of pathologies is associated with each of these tissues and therapeutic interventions, surgery or replacement may be necessary. A precise knowledge of the mechanical properties of these tissues is thus required in order to understand their functioning in native conditions, to be able to elaborate some prostheses, or to design appropriate surgical training tools. These tissues may undergo expansions or contractions (peristalsis) and are exposed to internal pressures. The wall of tubular organs is organized in different layers, and each layer consists of various cell types and extra-cellular matrix, depending on the physiological functions that the organ has to fulfil. This yields anisotropic and compliant structures. In inflation experiments, the linear elasticity approach is acceptable as long as the organ’s inflation remains moderate. In this paper, elasticity laws are revisited and supplemented in order to show that, coupled with modern experimental characterization tools, they provide useful information (compliances, directional Young moduli, Poisson ratios) for the design of artificial tubular organs. The importance of a precise determination of the wall thickness and its evolution during inflation is pointed out.
References
[1]
Fung, Y.C. (1993) Biomechanics: Mechanical Properties of Living Tissues. 2nd Edition, Springer.
[2]
Bergel, D.H. (1961) The Static Elastic Properties of the Arterial Wall. The Journal of Physiology, 156, 445-457. https://doi.org/10.1113/jphysiol.1961.sp006686
[3]
Boys, A.J., Barron, S.L., Tilev, D. and Owens, R.M. (2020) Building Scaffolds for Tubular Tissue Engineering. Frontiers in Bioengineering and Biotechnology, 8, Article ID: 589960. https://doi.org/10.3389/fbioe.2020.589960
[4]
Pien, N., Palladino, S., Copes, F., Candiani, G., Dubruel, P., Van Vlierberghe, S., et al. (2021) Tubular Bioartificial Organs: From Physiological Requirements to Fabrication Processes and Resulting Properties. A Critical Review. Cells Tissues Organs, 211, 420-446. https://doi.org/10.1159/000519207
[5]
Dobrin, P.B. and Doyle, J.M. (1970) Vascular Smooth Muscle and the Anisotropy of Dog Carotid Artery. Circulation Research, 27, 105-119. https://doi.org/10.1161/01.res.27.1.105
[6]
Dobrin, P.B. (1986) Biaxial Anisotropy of Dog Carotid Artery: Estimation of Circumferential Elastic Modulus. Journal of Biomechanics, 19, 351-358. https://doi.org/10.1016/0021-9290(86)90011-4
[7]
Lillie, M.A., Shadwick, R.E. and Gosline, J.M. (2010) Mechanical Anisotropy of Inflated Elastic Tissue from the Pig Aorta. Journal of Biomechanics, 43, 2070-2078. https://doi.org/10.1016/j.jbiomech.2010.04.014
[8]
Abbott, W.M., Megerman, J., Hasson, J.E., L’Italien, G. and Warnock, D.F. (1987) Effect of Compliance Mismatch on Vascular Graft Patency. Journal of Vascular Surgery, 5, 376-382. https://doi.org/10.1016/0741-5214(87)90148-0
[9]
Li, C., Wang, F., Douglas, G., Zhang, Z., Guidoin, R. and Wang, L. (2017) Comprehensive Mechanical Characterization of PLA Fabric Combined with PCL to Form a Composite Structure Vascular Graft. Journal of the Mechanical Behavior of Biomedical Materials, 69, 39-49. https://doi.org/10.1016/j.jmbbm.2016.11.005
[10]
Castillo-Cruz, O., Pérez-Aranda, C., Gamboa, F., Cauich-Rodríguez, J.V., Mantovani, D. and Avilés, F. (2018) Prediction of Circumferential Compliance and Burst Strength of Polymeric Vascular Grafts. Journal of the Mechanical Behavior of Biomedical Materials, 79, 332-340. https://doi.org/10.1016/j.jmbbm.2017.12.031
[11]
Camasão, D.B. and Mantovani, D. (2021) The Mechanical Characterization of Blood Vessels and Their Substitutes in the Continuous Quest for Physiological-Relevant Performances. A Critical Review. Materials Today Bio, 10, Article ID: 100106. https://doi.org/10.1016/j.mtbio.2021.100106
[12]
Saksena, R., Gao, C., Wicox, M. and de Mel, A. (2016) Tubular Organ Epithelialisation. Journal of Tissue Engineering, 7. https://doi.org/10.1177/2041731416683950
[13]
Patel, B., Gizzi, A., Hashemi, J., Awakeem, Y., Gregersen, H. and Kassab, G. (2022) Biomechanical Constitutive Modeling of the Gastrointestinal Tissues: A Systematic Review. Materials & Design, 217, Article ID: 110576. https://doi.org/10.1016/j.matdes.2022.110576
[14]
Durcan, C., Hossain, M., Chagnon, G., Perić, D. and Girard, E. (2023) Mechanical Experimentation of the Gastrointestinal Tract: A Systematic Review. Biomechanics and Modeling in Mechanobiology, 23, 23-59. https://doi.org/10.1007/s10237-023-01773-8
[15]
Jeong, H., Nam, H., Jang, J. and Lee, S. (2020) 3D Bioprinting Strategies for the Regeneration of Functional Tubular Tissues and Organs. Bioengineering, 7, Article No. 32. https://doi.org/10.3390/bioengineering7020032
[16]
de Mel, A., Yap, T., Cittadella, G., Hale, L.R., Maghsoudlou, P., de Coppi, P., et al. (2015) A Potential Platform for Developing 3D Tubular Scaffolds for Paediatric Organ Development. Journal of Materials Science: Materials in Medicine, 26, Article No. 141. https://doi.org/10.1007/s10856-015-5477-4
[17]
Farhat, W., Chatelain, F., Marret, A., Faivre, L., Arakelian, L., Cattan, P., et al. (2021) Trends in 3D Bioprinting for Esophageal Tissue Repair and Reconstruction. Biomaterials, 267, Article ID: 120465. https://doi.org/10.1016/j.biomaterials.2020.120465
[18]
Lee, H., Jang, T., Han, G., Kim, H. and Jung, H. (2021) Freeform 3D Printing of Vascularized Tissues: Challenges and Strategies. Journal of Tissue Engineering, 12. https://doi.org/10.1177/20417314211057236
[19]
Bernal, M., Urban, M.W., Rosario, D., Aquino, W. and Greenleaf, J.F. (2011) Measurement of Biaxial Mechanical Properties of Soft Tubes and Arteries Using Piezoelectric Elements and Sonometry. Physics in Medicine and Biology, 56, 3371-3386. https://doi.org/10.1088/0031-9155/56/11/012
[20]
Macrae, R.A., Miller, K. and Doyle, B.J. (2016) Methods in Mechanical Testing of Arterial Tissue: A Review. Strain, 52, 380-399. https://doi.org/10.1111/str.12183
[21]
Sanders, S.N., Lopata, R.G.P., van Breemen, L.C.A., van de Vosse, F.N. and Rutten, M.C.M. (2020) A Novel Technique for the Assessment of Mechanical Properties of Vascular Tissue. Biomechanics and Modeling in Mechanobiology, 19, 1585-1594. https://doi.org/10.1007/s10237-020-01292-w
[22]
Maeda, E., Ando, Y., Takeshita, K. and Matsumoto, T. (2022) Through the Cleared Aorta: Three-Dimensional Characterization of Mechanical Behaviors of Rat Thoracic Aorta under Intraluminal Pressurization Using Optical Clearing Method. Scientific Reports, 12, Article No. 8632. https://doi.org/10.1038/s41598-022-12429-5
[23]
Urban, M.W. (2023) Understanding Arterial Biomechanics with Ultrasound and Waveguide Models. Acoustics Today, 19, 46-54. https://doi.org/10.1121/at.2023.19.1.46
[24]
Sommer, G., Schriefl, A., Zeindlinger, G., Katzensteiner, A., Ainödhofer, H., Saxena, A., et al. (2013) Multiaxial Mechanical Response and Constitutive Modeling of Esophageal Tissues: Impact on Esophageal Tissue Engineering. Acta Biomaterialia, 9, 9379-9391. https://doi.org/10.1016/j.actbio.2013.07.041
[25]
Assoul, N., Flaud, P., Chaouat, M., Letourneur, D. and Bataille, I. (2008) Mechanical Properties of Rat Thoracic and Abdominal Aortas. Journal of Biomechanics, 41, 2227-2236. https://doi.org/10.1016/j.jbiomech.2008.04.017
[26]
Takeda, T., Kassab, G., Liu, J., Puckett, J.L., Mittal, R.R. and Mittal, R.K. (2002) A Novel Ultrasound Technique to Study the Biomechanics of the Human Esophagus in Vivo. American Journal of Physiology-Gastrointestinal and Liver Physiology, 282, G785-G793. https://doi.org/10.1152/ajpgi.00394.2001
[27]
Patel, D.J., Janicki, J.S. and Carew, T.E. (1969) Static Anisotropic Elastic Properties of the Aorta in Living Dogs. Circulation Research, 25, 765-779. https://doi.org/10.1161/01.res.25.6.765
[28]
Nahon, D., Lee, J.M. and Wilson, G.J. (1986) A Two-Dimensional Incremental Study of the Static Mechanical Properties of Vascular Grafts. Clinical Materials, 1, 177-197. https://doi.org/10.1016/s0267-6605(86)80031-2
[29]
Cox, R.H. (1975) Anisotropic Properties of the Canine Carotid Artery in Vitro. Journal of Biomechanics, 8, 293-300. https://doi.org/10.1016/0021-9290(75)90081-0
[30]
Sugita, S., Kato, M., Wataru, F. and Nakamura, M. (2019) Three-Dimensional Analysis of the Thoracic Aorta Microscopic Deformation during Intraluminal Pressurization. Biomechanics and Modeling in Mechanobiology, 19, 147-157. https://doi.org/10.1007/s10237-019-01201-w
[31]
Skacel, P. and Bursa, J. (2022) Poisson’s Ratio and Compressibility of Arterial Wall—Improved Experimental Data Reject Auxetic Behaviour. Journal of the Mechanical Behavior of Biomedical Materials, 131, Article ID: 105229. https://doi.org/10.1016/j.jmbbm.2022.105229
[32]
Holzapfel, G.A., Gasser, T.C. and Ogden, R.W. (2000) A New Constitutive Framework for Arterial Wall Mechanics and a Comparative Study of Material Models. Journal of Elasticity and the Physical Science of Solids, 61, 1-48. https://doi.org/10.1023/a:1010835316564