Abstract
Aortic dissections progress, in part, by delamination of the wall. Previous experiments on cut-open segments of aorta demonstrated that fluid injected within the wall delaminates the aorta in two distinct modes: stepwise progressive tearing in the abdominal aorta and a more prevalent sudden mode of tearing in the thoracic aorta that can also manifest in other regions. A microstructural understanding that delineates these two modes of tearing has remained wanting. We implemented a phase-field finite-element model of the aortic wall, motivated in part by two-photon imaging, and found correlative relations for the maximum pressure prior to tearing as a function of local geometry and material properties. Specifically, the square of the pressure of tearing relates directly to both tissue stiffness and the critical energy of tearing and inversely to the square root of the torn area; this correlation explains the sudden mode of tearing and, with the microscopy, suggests a mechanism for progressive tearing. Microscopy also confirmed that thick interlamellar radial struts are more abundant in the abdominal region of the aorta, where progressive tearing was observed previously. The computational results suggest that structurally significant radial struts increase tearing pressure by two mechanisms: confining the fluid by acting as barriers to flow and increasing tissue stiffness by holding the adjacent lamellae together. Collectively, these two phase-field models provide new insights into the mechanical factors that can influence intramural delaminations that promote aortic dissection.
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References
Ahmadzadeh H, Rausch MK, Humphrey JD (2019) Modeling lamellar disruption within the aortic wall using a particle-based approach. Sci Rep 9:15320. https://doi.org/10.1038/s41598-019-51558-2
Alnæs M, Blechta J, Hake J, et al (2015) The FEniCS project version 1.5. Archive of Numerical Software. https://doi.org/10.11588/ans.2015.100.20553
Ambrosio L, Tortorelli VM (1990) Approximation of functional depending on jumps by elliptic functional via Γ-convergence. Commun Pur Appl Math 43:999–1036. https://doi.org/10.1002/cpa.3160430805
Bonet J, Gil AJ, Wood RD (2016) Nonlinear solid mechanics for finite element analysis: statics. Cambridge University Press, Cambridge, UK
Borden MJ, Verhoosel CV, Scott MA et al (2012) A phase-field description of dynamic brittle fracture. Comput Method Appl M 217–220:77–95. https://doi.org/10.1016/j.cma.2012.01.008
Bourdin B, Francfort GA, Marigo J-J (2008) The variational approach to fracture. J Elast 91:5–148. https://doi.org/10.1007/s10659-007-9107-3
Carson MW, Roach MR (1990) The strength of the aortic media and its role in the propagation of aortic dissection. J Biomech 23:579–588. https://doi.org/10.1016/0021-9290(90)90050-D
Cikach FS, Koch CD, Mead TJ et al (2018) Massive aggrecan and versican accumulation in thoracic aortic aneurysm and dissection. JCI Insight https://doi.org/10.1172/jci.insight.97167
Clouse WD, Hallett JW, Schaff HV et al (2004) Acute aortic dissection: population-based incidence compared with degenerative aortic aneurysm rupture. Mayo Clin Proc 79:176–180. https://doi.org/10.4065/79.2.176
Dingemans KP, Teeling P, van der Wal AC, Becker AE (2006) Ultrastructural pathology of aortic dissections in patients with Marfan syndrome: Comparison with dissections in patients without Marfan syndrome. Cardiovasc Pathol 15:203–212. https://doi.org/10.1016/j.carpath.2006.03.004
Elefteriades JA (2008) Thoracic aortic aneurysm: reading the enemy’s playbook. Curr Probl Cardiol 33:203–277. https://doi.org/10.1016/j.cpcardiol.2008.01.004
Evangelista A, Isselbacher EM, Bossone E et al (2018) Insights from the International Registry of Acute Aortic Dissection. Circulation 137:1846–1860. https://doi.org/10.1161/CIRCULATIONAHA.117.031264
Gasser TC, Holzapfel GA (2006) Modeling the propagation of arterial dissection. Eur J Mech A-Solid 25:617–633. https://doi.org/10.1016/j.euromechsol.2006.05.004
Gent AN (2012) Engineering with rubber: how to design rubber components. Hanser Publishers, Munich, Germany
Gent AN, Lewandowski LH (1987) Blow-off pressures for adhering layers. J Appl Polym Sci 33:1567–1577. https://doi.org/10.1002/app.1987.070330512
Griffith AA (1921) VI. The phenomena of rupture and flow in solids. Philos Trans R Soc A 221:163–198. https://doi.org/10.1098/rsta.1921.0006
Gültekin O, Hager SP, Dal H, Holzapfel GA (2019) Computational modeling of progressive damage and rupture in fibrous biological tissues: application to aortic dissection. Biomech Model Mechanobiol 18:1607–1628. https://doi.org/10.1007/s10237-019-01164-y
Haskett D, Johnson G, Zhou A et al (2010) Microstructural and biomechanical alterations of the human aorta as a function of age and location. Biomech Model Mechanobiol 9:725–736. https://doi.org/10.1007/s10237-010-0209-7
Hirst AE, Johns VJ (1962) Experimental dissection of media of aorta by pressure. Circ Res 10:897–903. https://doi.org/10.1161/01.RES.10.6.897
Howard DPJ, Amitava B, Fairhead JF et al (2013) Population-based study of incidence and outcome of acute aortic dissection and premorbid risk factor control. Circulation 127:2031–2037. https://doi.org/10.1161/CIRCULATIONAHA.112.000483
Hughes TJR (2012) The finite element method: Linear static and dynamic finite element analysis. Dover Publication, Mineola, New York
Humphrey JD, Schwartz MA, George T, Milewicz DM (2015) Role of mechanotransduction in vascular biology. Circ Res 116:1448–1461. https://doi.org/10.1161/CIRCRESAHA.114.304936
Humphrey JD (2013) Possible mechanical roles of glycosaminoglycans in thoracic aortic dissection and associations with dysregulated TGF-β. J Vasc Res 50:1–10. https://doi.org/10.1159/000342436
Landenhed M, Gunnar Engström, Anders Gottsäter et al (2015) Risk profiles for aortic dissection and ruptured or surgically treated aneurysms: a prospective cohort study. J Am Heart Assoc 4:e001513. https://doi.org/10.1161/JAHA.114.001513
Li B, Bouklas N (2020) A variational phase-field model for brittle fracture in polydisperse elastomer networks. Int J Solids Struct 182–183:193–204. https://doi.org/10.1016/j.ijsolstr.2019.08.012
MacLean NF, Dudek NL, Roach MR (1999) The role of radial elastic properties in the development of aortic dissections. J Vasc Surg 29:703–710. https://doi.org/10.1016/S0741-5214(99)70317-4
Miehe C, Welschinger F, Hofacker M (2010) Thermodynamically consistent phase-field models of fracture: Variational principles and multi-field FE implementations. Int J Numer Meth Eng 83:1273–1311. https://doi.org/10.1002/nme.2861
Mohan D, Melvin JW (1982) Failure properties of passive human aortic tissue. I—Uniaxial tension tests. J Biomech 16:31–44. https://doi.org/10.1016/0021-9290(83)90044-1
Mohan D, Melvin JW (1983) Failure properties of passive human aortic tissue. II—Biaxial tension tests. J Biomech 15:887–902. https://doi.org/10.1016/0021-9290(82)90055-0
Nienaber CA, Clough RE, Sakalihasan N et al (2016) Aortic dissection Nat Rev Dis Primers 2:1–18. https://doi.org/10.1038/nrdp.2016.53
O’Connell MK, Murthy S, Phan S et al (2008) The three-dimensional micro- and nanostructure of the aortic medial lamellar unit measured using 3D confocal and electron microscopy imaging. Matrix Biol 27:171–181. https://doi.org/10.1016/j.matbio.2007.10.008
Pasta S, Phillippi JA, Gleason TG, Vorp DA (2012) Effect of aneurysm on the mechanical dissection properties of the human ascending thoracic aorta. J Thorac Cardiovasc Surg 143:460–467. https://doi.org/10.1016/j.jtcvs.2011.07.058
Purslow PP (1983) Positional variations in fracture toughness, stiffness and strength of descending thoracic pig aorta. J Biomech 16:947–953. https://doi.org/10.1016/0021-9290(83)90058-1
Rivlin RS, Thomas AG (1953) Rupture of rubber. I. Characteristic energy for tearing. J Polym Sci 10:291–318. https://doi.org/10.1002/pol.1953.120100303
Roach MR, Song SH (1994) Variations in strength of the porcine aorta as a function of location. Clin Invest Med 17:308–318
Robertson JS, Smith KV (1948) An analysis of certain factors associated with the production of experimental dissection of the aortic media, in relation to the pathogenesis of dissecting aneurysm. J Pathol Bacteriol 60:43–49. https://doi.org/10.1002/path.1700600105
Roccabianca S, Ateshian GA, Humphrey JD (2014a) Biomechanical roles of medial pooling of glycosaminoglycans in thoracic aortic dissection. Biomech Model Mechanobiol 13:13–25. https://doi.org/10.1007/s10237-013-0482-3
Roccabianca S, Figueroa CA, Tellides G, Humphrey JD (2014b) Quantification of regional differences in aortic stiffness in the aging human. J Mech Behav Biomed 29:618–634. https://doi.org/10.1016/j.jmbbm.2013.01.026
Shah SB, Witzenburg C, Hadi MF et al (2014) Prefailure and failure mechanics of the porcine ascending thoracic aorta: experiments and a multiscale model. J Biomech Eng 136:021028. https://doi.org/10.1115/1.4026443
Shen YH, Lu HS, LeMaire Scott A, Alan D (2019) Unfolding the story of proteoglycan accumulation in thoracic aortic aneurysm and dissection. Arterioscler Thromb Vasc Biol 39:1899–1901. https://doi.org/10.1161/ATVBAHA.119.313279
Sherifova S, Holzapfel GA (2019) Biomechanics of aortic wall failure with a focus on dissection and aneurysm: A review. Acta Biomater 99:1–17. https://doi.org/10.1016/j.actbio.2019.08.017
Sneddon IN (1946) The distribution of stress in the neighbourhood of a crack in an elastic solid. Proc R Soc Lond 187:229–260. https://doi.org/10.1098/rspa.1946.0077
Sommer G, Gasser TC, Regitnig P et al (2008) Dissection properties of the human aortic media: an experimental study. J Biomech Eng 130:021007. https://doi.org/10.1115/1.2898733
Sommer G, Sherifova S, Oberwalder PJ et al (2016) Mechanical strength of aneurysmatic and dissected human thoracic aortas at different shear loading modes. J Biomech 49:2374–2382. https://doi.org/10.1016/j.jbiomech.2016.02.042
Tam ASM, Catherine Sapp M, Roach MR (1998) The effect of tear depth on the propagation of aortic dissections in isolated porcine thoracic aorta. J Biomech 31:673–676. https://doi.org/10.1016/S0021-9290(98)00058-X
Tanné E, Li T, Bourdin B et al (2018) Crack nucleation in variational phase-field models of brittle fracture. J Mech Phys Solids 110:80–99. https://doi.org/10.1016/j.jmps.2017.09.006
Tong J, Cheng Y, Holzapfel GA (2016) Mechanical assessment of arterial dissection in health and disease: Advancements and challenges. J Biomech 49:2366–2373. https://doi.org/10.1016/j.jbiomech.2016.02.009
Tsamis A, Pal S, Phillippi JA et al (2014) Effect of aneurysm on biomechanical properties of “radially-oriented” collagen fibers in human ascending thoracic aortic media. J Biomech 47:3820–3824. https://doi.org/10.1016/j.jbiomech.2014.10.024
Vande Geest JP, Sacks MS, Vorp DA (2004) Age dependency of the biaxial biomechanical behavior of human abdominal aorta. J Biomech Eng 126:815–822. https://doi.org/10.1115/1.1824121
Wang L, Roper SM, Hill NA, Luo X (2017) Propagation of dissection in a residually-stressed artery model. Biomech Model Mechanobiol 16:139–149. https://doi.org/10.1007/s10237-016-0806-1
Weiss D, Cavinato C, Gray A, et al (2020) Mechanics-driven mechanobiological mechanisms of arterial tortuosity. Sci Adv 6:eabd3574. https://doi.org/10.1126/sciadv.abd3574
Williams ML (1969) The continuum interpretation for fracture and adhesion. J Appl Polym Sci 13:29–40. https://doi.org/10.1002/app.1969.070130105
Wriggers P (2008) Special finite elements for continua. In: Wriggers P (eds) Nonlinear finite element methods, 1st edn. Springer, Berlin, Heidelberg, pp 399–460
Wu D, Shen YH, Russell L et al (2013) Molecular mechanisms of thoracic aortic dissection. J Surg Res 184:907–924. https://doi.org/10.1016/j.jss.2013.06.007
Yu X, Suki B, Zhang Y (2020) Avalanches and power law behavior in aortic dissection propagation. Sci Adv 6:eaaz1173. https://doi.org/10.1126/sciadv.aaz1173
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This work was supported, in part, by a grant from the US National Institutes of Health (U01 HL142518).
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Ban, E., Cavinato, C. & Humphrey, J.D. Differential propensity of dissection along the aorta. Biomech Model Mechanobiol 20, 895–907 (2021). https://doi.org/10.1007/s10237-021-01418-8
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DOI: https://doi.org/10.1007/s10237-021-01418-8