Biomechanics of aortic wall failure with a focus on dissection and aneurysm: A review

Abstract

Aortic dissections and aortic aneurysms are fatal events characterized by structural changes to the aortic wall. The maximum diameter criterion, typically used for aneurysm rupture risk estimations, has been challenged by more sophisticated biomechanically motivated models in the past. Although these models are very helpful for the clinicians in decision-making, they do not attempt to capture material failure. Following a short overview of the microstructure of the aorta, we analyze the failure mechanisms involved in the dissection and rupture by considering also traumatic rupture. We continue with a literature review of experimental studies relevant to quantify tissue strength. More specifically, we summarize more extensively uniaxial tensile, bulge inflation and peeling tests, and we also specify trouser, direct tension and in-plane shear tests. Finally we analyze biomechanically motivated models to predict rupture risk. Based on the findings of the reviewed studies and the rather large variations in tissue strength, we propose that an appropriate material failure criterion for aortic tissues should also reflect the microstructure in order to be effective. STATEMENT OF SIGNIFICANCE: Aortic dissections and aortic aneurysms are fatal events characterized by structural changes to the aortic wall. Despite the advances in medical, biomedical and biomechanical research, the mortality rates of aneurysms and dissections remain high. The present review article summarizes experimental studies that quantify the aortic wall strength and it discusses biomechanically motivated models to predict rupture risk. We identified contradictory observations and a large variation within and between data sets, which may be due to biological variations, different sample sizes, differences in experimental protocols, etc. Based on the findings of the reviewed literature and the rather large variations in tissue strength, it is proposed that an appropriate criterion for aortic failure should also reflect the microstructure.

Keywords: Aortic aneurysm; Aortic dissection; Aortic failure; Aortic microstructure; Bulge inflation test; Peeling test; Rupture risk; Tissue strength; Uniaxial tensile test.

Fig. 1.

(a) Anatomy of the aorta with some of its branches; (b) sketch of a dissected wall with arrows indicating the blood flow.

Fig. 2.

Structure of the aorta: (a) healthy but aged aortic wall with non-atherosclerotic intimal thickening composed of three layers – intima (I), media (M) and adventitia (A). Republished with permission from Gasser et al. [40]; (b) layered collagen architecture of a healthy and aged abdominal aorta – more specifically the top image depicts the out-of-plane structure in the circumferential-radial plane, while the three images at the bottom show in-plane sections of the intima (I), media (M) and adventitia (A) (white scale bars corresponding to 100 μm. Republished with permission from Niestrawska et al. [89]; (c) 3D microstructure of an aortic media consisting of several lamellar units –circumferentially-oriented radially-tilted smooth muscle cells (SMCs) with elliptical nuclei (N) sandwiched between elastic lamellas (EL) surrounded by a dense network of interlamellar elastin fibers (IEFs shown with black arrows), elastin struts (ES), and reinforced elastin pores (EP). Reprinted from O’Connell et al. [94], with permission from Elsevier; (d) schematic representation of two SMCs and two fenestrated EL with their interconnections – more specifically, collagen fibers (Coll) are closely associated with EL, surface ridges of the left SMC are connected to both EL via elastin protrusions, right SMC is connected to the lower El via oxytalan fiber (Ox), and larger deposits (D) containing collagen and heparan sulfate proteoglycan are found at indentations of the cell surface. Reprinted from Dingemans et al. [29], with permission from John Wiley and Sons.

Fig. 3.

Microstructural changes due to pathological formations in human thoracic aortas with stars indicating mucoid accumulation areas (proteoglycan pools): (a), (b) disorganized collagen network visualized by (a) a histological section stained by picrosirius - collagen framework is disorganized - and (b) scanning electron microscopy (SEM); (c), (d) SEM images showing a lamellar structure disrupted probably by the proteoglycan pools (star) (Adv = Adventitia; End = endothelium coverage of the luminal face). Reprinted from Borges et al. [6] (Copyright © 2013 Karger Publishers, Basel, Switzerland); (e), (f) histological sections stained byAlcian blue showing (e) a pathological aorta with areas of mucoid accumulations (stars) - inset shows immunostaining for α-actin demonstrating the absence of SMCs inside the mucoid area; (f) control aorta where the space between elastic lamellae (arrow) is occupied by SMCs, collagen, and a normal amount of mucoid substance (light blue). Reprinted from Borges et al. [8], with permission from Elsevier; (g), (h) SEM images depicting the elastic fiber architecture of human aortic medias from (g) an aortic dissection patient and (h) a control subject (black scale bars indicate 20 μm. Reprinted from Nakashima [87] (licensed under CC BY-NC-SA 2.1 JP).

Fig. 4.

Pressure volume curves to create a bleb in the thoracic and abdominal sections of the aorta. Reprinted from Roach & Song [114], with permission from Clin. Invest. Med.

Fig. 5.

Initiation/propagation of aortic dissections due to shear stresses: (a)-(c) cracks visible after a block shear test, where the white areas are openings in the tissue. Reprinted from Haslach, Jr. et al. [47] with permission from Springer Nature; (a), (b) are slices in the circumferential-longitudinal plane where the horizontal direction is longitudinal - (a) circumferential deformation parallel to the collagen fibers and (b) longitudinal deformation; (c) slice in the radial-circumferential plane after circumferential deformation, where the horizontal direction is circumferential; (d) cracks visible as black zones between the lamellae in the radial-circumferential plane after an in-plane shear test in the circumferential direction. Reprinted from Sommer et al. [131], with permission from Elsevier; (e) cracks that occurred during a uniaxial test indicated by black arrows. Reprinted from Helfenstein-Didier et al. [50], with permission from Elsevier.

Fig. 6.

Aortic dissection and rupture due to traumatic injury. Reprinted from Prijon & Ermenc [106], with permission from Elsevier: (a) case presenting multiple ruptures: intramural and transmural, latter both in circumferential and longitudinal directions indicated by white arrows; (b) intramural rupture of the intima; (c) intramural rupture of the intima and the media.

Fig. 7.

Experimental tests typically used to quantify the failure properties of aortas: (a) bone-shaped specimen for a uniaxial tensile test with load F; (b) bulge inflation test with pressure load p; (c) peeling test; (d) trouser test, as used in, e.g., Purslow [107]; (e) direct tension test to quantify radial strength, as used in, e.g., Sommer et al. [130,131]; (f) in-plane shear test with the sheared plane indicated in gray, as used in, e.g., Sommer et al. [131]. Black arrows and dashed lines indicate the load direction and the incision, respectively. Tests (a), (c), (d) and (f) can be performed in any tissue direction in the tangential plane.

Fig. 8.

Stress-strain data of ascending thoracic aortic aneurysm (ATAA) and control specimens taken from the anterior region with (a) circumferential and (b) longitudinal orientation obtained from uniaxial tensile tests. Data show a large variability in failure properties. Reprinted from Iliopoulos et al. [56], with permission from Elsevier.

Fig. 9.

Histological images (Elastica van Gieson) of the dissection tips obtained from a peeling test of an aortic media during peeling in (a) circumferential and (b) longitudinal directions. Republished from Sommer et al. [130], Copyright © 2008 ASME, permission conveyed through CCC, Inc. The images highlight the irreversible mechanism of the separation at the microscopic level. (c) Schematic of fiber bridging failure; the matrix is already separated but still connected by an unruptured fiber (above); force-separation law (F vs Δ) for a collagen fiber bridge with nonlinear loading and linear post peak behavior starting at F_max and related Δ_p (below) - modes of fiber deformation and failure are depicted in the insets. Shaded region represents the energy U_f required for failure of the fiber bridge. Reprinted from Pal et al. [96], with permission from Elsevier.