Fiber micro-architecture in the longitudinal-radial and circumferential-radial planes of ascending thoracic aortic aneurysm media

Abstract

It was recently demonstrated by our group that the delamination strength of ascending thoracic aortic aneurysms (ATAA) was lower than that of control (CTRL, non-aneurysmal) ascending thoracic aorta (ATA), and the reduced strength was more pronounced among bicuspid (BAV) vs. tricuspid aortic valve (TAV) patients, suggesting a different risk of aortic dissection for BAV patients. We hypothesized that aortic valve morphologic phenotype predicts fiber micro-architectural anomalies in ATA. To test the hypothesis, we characterized the micro-architecture in the longitudinal-radial (Z-RAD) and circumferential-radial (Θ-RAD) planes of human ATA tissue that was artificially dissected medially. The outer and inner-media of CTRL-ATA, BAV-ATAA and TAV-ATAA were imaged using multi-photon microscopy in the Z-RAD and Θ-RAD planes to observe collagen and elastin. Micrographs were processed using an image-based tool to quantify several micro-architectural characteristics. In the outer-media of BAV-ATAA, elastin was more undulated and less aligned about the Θ-axis when compared with CTRL-ATA, which is consistent with increased tensile stretch at inflection point of Θ-strips of adventitial-medial half of BAV-ATAA (1.28) when compared with CTRL-ATA (1.13). With increasing age, collagen became more undulated about the Z-axis within the outer-media of TAV-ATAA, and elastin became more oriented in the Z-axis and collagen less radially-oriented within the inner-media of TAV-ATAA. This discrepancy in the micro-architecture with fibers in the inner layers being more stretched and with disrupted radially-oriented components than fibers in the outer layers may be associated with the development, progression and vascular remodeling in aneurysms arising in TAV patients.

Failure of the Porcine Ascending Aorta: Multidirectional Experiments and a Unifying Microstructural Model

“…Network parameters were selected to reflect the biological roles of each component and were adjusted to match the experimental results. This approach was successful in matching a wide range of tissue mechanical tests, including one-radial extension to failure-that was not used during the fitting process, and it has the potential to be extended to the more disorganized (and thus more complex) architecture of the aneurysm, especially as better imaging and image-based modeling methods emerge [67,68]. The work of Pal et al [61] represents an excellent example of this approach, developing a theoretical model of peel failure based on known structure.…”

Structure-based constitutive model can accurately predict planar biaxial properties of aortic wall tissue

“…Since only <5% of collagen fibers point in a radial direction [56], and as used previously [52], a planar von Mises distribution function was also used in the present study to capture collagen orientations. Avoiding introducing a three-dimensional von Mises or Bingham distribution function also leads also to a considerably faster numerical implementation of the model.…”

“…Several microscopy techniques such as classical microscopy [16], polarized light microscopy (PLM) [13,14], multi-photon microscopy [56,57] or small-angle light scattering [15] together with various imageprocessing techniques (see Ref. [16] and references therein) have been suggested to study the collagen organization in the arterial wall.…”

Identification of vessel wall degradation in ascending thoracic aortic aneurysms with OCT

“…Aortic dissections and ascending aorta aneurysms share the same histopathologic features, situated at the medial layer namely, increase in mucoid substance, fragmentation of elastic fibers, and apparent reduction in the number of smooth muscle cells [2]. A possible mechanism for dissection [3] is that blood pressure-induced stresses exceed the adhesive strength that holds the elastic layers together [4]. The resistance to delamination may be affected by the interlaminar elastin and collagen fibers which are radially-orientated.…”

“…The conventional histopathological analysis provides the gold standard to evaluate the quality of the aortic wall [2], but its implementation is not straightforward during intervention. Optical techniques such as multiphoton microscopy [3,4] have assessed the degradation of the aortic wall with penetrations of 200μm and, when combined with coherent anti-Stokes Raman spectroscopy is able to distinguish collagen from cholesterol in atherosclerotic arterial tissue [7] quantifying the fiber size, distribution and anisotropy of collagen in healthy arterial wall and in atherosclerotic plaque using image pattern evaluation algorithms. Optical Coherence Tomography, able to provide depth penetrations of 2 mm, has been also applied to arterial wall analysis but mainly focused in the assessment of different types of atherosclerotic plaques in coronary arteries (fibrous, fibrocalcific, lipid rich) [8][9][10] more than in aortic arteries.…”