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(A, B) Elastin and (C, D) collagen contents in the entire wall of circumferential (CIRC) and longitudinal (LONG) left coronary sinus (LCS), right coronary sinus (RCS), and noncoronary sinus (NCS) sections from aneurysmal and control subjects for young and old subjects. yz *Signi fi cant differences against control, old, and LONG specimens, respectively. Inside parentheses are the number of specimens used for content measurements. (Black bars 1⁄4 aneurysmal CIRC; white bars 1⁄4 aneurysmal LONG; dark gray bars 1⁄4 control CIRC; light gray bars 1⁄4 control LONG.)
Source publication
Aortic root aneurysms are relatively uncommon but their rupture is a detrimental event with acute hemodynamic compromise and high mortality, and there are few available data on their mechanical properties, although aneurysm rupture occurs when hemodynamic stresses exceed wall strength. This study aimed to fill this gap by examining the effect of an...
Contexts in source publication
Context 1
... contents did not differ notably between aneurysmal and control sinuses, but invariably declined with age ( Fig 5). Collagen content correlated positively with failure stress (r ¼ 0.67, p < 0.001) and peak elastic modulus (r ¼ 0.60, p < 0.001), as did elastin content with failure stretch (r ¼ 0.49, p < 0.001) and stress (r ¼ 0.45, p < 0.001). ...
Context 2
... age-related differences in mechanical properties were similar for both aneurysmal and control tissue, with the younger specimens presenting greater tensile strength and maximum tissue stiffness (Fig 4) along with greater extensibility (data not shown), justified by their higher elastin and collagen contents (Fig 5). These results No-load thickness of fresh tissue from aneurysmal subjects (black bars) and control subjects (gray bars) for (A) young group and (B) old group. ...
Context 3
... contents did not differ notably between aneurysmal and control sinuses, but invariably declined with age ( Fig 5). Collagen content correlated positively with failure stress (r ¼ 0.67, p < 0.001) and peak elastic modulus (r ¼ 0.60, p < 0.001), as did elastin content with failure stretch (r ¼ 0.49, p < 0.001) and stress (r ¼ 0.45, p < 0.001). ...
Context 4
... age-related differences in mechanical properties were similar for both aneurysmal and control tissue, with the younger specimens presenting greater tensile strength and maximum tissue stiffness (Fig 4) along with greater extensibility (data not shown), justified by their higher elastin and collagen contents (Fig 5). These results No-load thickness of fresh tissue from aneurysmal subjects (black bars) and control subjects (gray bars) for (A) young group and (B) old group. ...
Context 5
... in the other sinuses of older subjects, failure stress and peak elastic modulus of aneurysmal tissue were smaller in the CIRC but greater in the LONG axis ( Fig 4), and material constants were essentially non- varying compared with control. Elastin/collagen contents did not differ notably between aneurysmal and control sinuses, but invariably declined with age (Fig 5). Collagen content correlated positively with failure stress ( r 1⁄4 0.67, p < 0.001) and peak elastic modulus ( r 1⁄4 0.60, p < 0.001), as did elastin content with failure stretch ( r 1⁄4 0.49, p < 0.001) and stress ( r 1⁄4 0.45, p < 0.001). Correlations between aneurysm diameter and all failure parameters were negative but weak ( r > À 0.3). The major fi nding of this study was that aneurysmal tissue showed less obvious directional differences in NCS, and near-similar stress-stretch curves, material constants, and failure properties in the right coronary sinus (RCS) and left coronary sinus (LCS) (Figs 3 and 4, Table 2), contrasting the direction-dependent properties in all healthy sinuses. Importantly, this mechanical adaptation seems to correlate with the histologic adaptation noted in those sinuses. Particularly, we observed that the aneurysmal RCS and LCS, and to a lesser extent the NCS, exhibited a complex microstructural organization with arbitrarily aligned lamellar units (Figs 6 and 7). The microstructure was more homogeneous in nonaneurysmal sinuses, albeit not to the extent of the ascending aorta, comprising elastic laminae, collagen bundles, and smooth muscle cells, all with uniform CIRC alignment [8]. Consideration of stresses in the sinus wall taken as a thin-walled structure (Laplace ’ s law) offers an explanation for this histomechanical adaptation of aneurysmal sinuses. Their isotropic properties are consistent with the more axisymmetric stresses (ie, the ratio of stresses in the CIRC and LONG axes is close to 1:1) exerted on them because of their more spherical shape, and so are the anisotropic (direction-dependent) properties of healthy sinuses with their nondilated bulb-shaped geometry, for which the stress ratio is between 1:1 and 1:2. The age-related differences in mechanical properties were similar for both aneurysmal and control tissue, with the younger specimens presenting greater tensile strength and maximum tissue stiffness (Fig 4) along with greater extensibility (data not shown), justi fi ed by their higher elastin and collagen contents (Fig 5). These results highlight the importance of using age-matched sinus tissues when considering differences between dilated and nondilated sinuses. We have earlier demonstrated that ascending aortic aneurysms are not associated with wall weakening [10]. Herein, the failure properties of NCS did not vary among aneurysmal and age-matched ...
Context 6
... in the other sinuses of older subjects, failure stress and peak elastic modulus of aneurysmal tissue were smaller in the CIRC but greater in the LONG axis ( Fig 4), and material constants were essentially non- varying compared with control. Elastin/collagen contents did not differ notably between aneurysmal and control sinuses, but invariably declined with age (Fig 5). Collagen content correlated positively with failure stress ( r 1⁄4 0.67, p < 0.001) and peak elastic modulus ( r 1⁄4 0.60, p < 0.001), as did elastin content with failure stretch ( r 1⁄4 0.49, p < 0.001) and stress ( r 1⁄4 0.45, p < 0.001). Correlations between aneurysm diameter and all failure parameters were negative but weak ( r > À 0.3). The major fi nding of this study was that aneurysmal tissue showed less obvious directional differences in NCS, and near-similar stress-stretch curves, material constants, and failure properties in the right coronary sinus (RCS) and left coronary sinus (LCS) (Figs 3 and 4, Table 2), contrasting the direction-dependent properties in all healthy sinuses. Importantly, this mechanical adaptation seems to correlate with the histologic adaptation noted in those sinuses. Particularly, we observed that the aneurysmal RCS and LCS, and to a lesser extent the NCS, exhibited a complex microstructural organization with arbitrarily aligned lamellar units (Figs 6 and 7). The microstructure was more homogeneous in nonaneurysmal sinuses, albeit not to the extent of the ascending aorta, comprising elastic laminae, collagen bundles, and smooth muscle cells, all with uniform CIRC alignment [8]. Consideration of stresses in the sinus wall taken as a thin-walled structure (Laplace ’ s law) offers an explanation for this histomechanical adaptation of aneurysmal sinuses. Their isotropic properties are consistent with the more axisymmetric stresses (ie, the ratio of stresses in the CIRC and LONG axes is close to 1:1) exerted on them because of their more spherical shape, and so are the anisotropic (direction-dependent) properties of healthy sinuses with their nondilated bulb-shaped geometry, for which the stress ratio is between 1:1 and 1:2. The age-related differences in mechanical properties were similar for both aneurysmal and control tissue, with the younger specimens presenting greater tensile strength and maximum tissue stiffness (Fig 4) along with greater extensibility (data not shown), justi fi ed by their higher elastin and collagen contents (Fig 5). These results highlight the importance of using age-matched sinus tissues when considering differences between dilated and nondilated sinuses. We have earlier demonstrated that ascending aortic aneurysms are not associated with wall weakening [10]. Herein, the failure properties of NCS did not vary among aneurysmal and age-matched ...
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Citations
... Furthermore, intimal tears in type-A dissection could be potentially missed or misclassified during prospective imaging of ascending aortic dilatation [8]. The ex vivo mechanical strength and material properties of proximal aortic aneurysms prior to and following dissection have been characterized in several experimental studies using uniaxial [10][11][12][13][14][15][16][17][18][19][20][21] and biaxial [22][23][24][25][26][27][28] testing of tissue specimens. Finite element analysis (FEA) has been employed to evaluate the biomechanical response of the diseased thoracic aorta [29], abdominal aorta [30], and cerebral vasculature [31], to cardiac pressure forces. ...
The risk of Type-A dissection is increased in subjects with connective tissue disorders and dilatation of the proximal aorta. The location and extents of vessel wall tears in these patients could be potentially missed during prospective imaging studies. The objective of the present study is to estimate the distribution of systolic wall stress in two exemplary cases of proximal dissection using finite element analysis (FEA) and evaluate the sensitivity of the distribution to the choice of anisotropic material model and root motion. FEA was performed for pre-dissection aortas, without prior knowledge of the origin and extents of vessel wall tear. The stress distribution was evaluated along the wall tear in the post-dissection aortas. The stress distribution was compared for the Fung and Holzapfel models with and without root motion. For the subject with spiral dissection, peak stress coincided with the origin of the tear in the sinotubular junction. For the case with root dissection, maximum stress was obtained at the distal end of the tear. The FEA predicted tear pressure was 20% higher for the subject with root dissection as compared to the case with spiral dissection. The predicted tear pressure was higher (9-11%) for root motions up to 10mm. The Holzapfel model predicted a tear pressure that was lower (8-15%) than the Fung model. The FEA results showed that both material response and root motion could potentially influence the predicted dissection pressure of the proximal aorta at least for conditions tested in this study.
... They are defined by wall stiffening and loss of extensibility, but our group raised the question a decade ago of whether aneurysm formation has in fact a degenerative effect on aortic wall strength. Previous studies from our group [38][39][40] suggested that aneurysms of the ascending aorta and aortic root are not related to wall weakening, only with reduced wall extensibility and stiffening. Our layer-specific data, identifying nonsignificant differences in intimal and adventitial (albeit reduced medial) failure stress and decreased failure stretch of all layers in TAV-ATAAs compared to non-aneurysmal aortas, further reinforce our previous observations while emphasizing the weakened integrity of the media in TAV-ATAAs. ...
Bicuspid aortic valve is the most common congenital cardiovascular defect, often associated with proximal aortic dilatation, and the ideal management strategy is debated. The inconsistency in previous and present guideline recommendations emphasizes the insufficiency of the maximal diameter as the sole criterion for prophylactic repair. Our ability to guide clinical decisions may improve through an understanding of the mechanical properties of ascending thoracic aortic aneurysms in bicuspid compared to tricuspid aortic valve patients and non-aneurysmal aortas, because dissection and rupture are aortic wall mechanical failures. Such an understanding of the mechanical properties has been attempted by several authors, and this article addresses whether there is a controversy in the accumulated knowledge. The available mechanical studies are briefly reviewed, discussing factors such as age, sex, and the region of mechanical examination that may be responsible for the lack of unanimity in the reported findings. The rationale for acquiring layer-specific properties is presented along with the main results from our recent study. No mechanical vulnerability of ascending thoracic aortic aneurysms was evidenced in bicuspid aortic valve patients, corroborating present conservative guidelines concerning the management of bicuspid aortopathy. Weakening and additional vulnerability was evidenced in aged patients and those with coexisting valve pathology, aortic root dilatation, hypertension, and hyperlipidemia. Discussion of these results from age- and sex-matched subjects, accounting for the region- and layer-specific aortic heterogeneity, in relation to intact wall results and histologic confirmation, helps to reconcile previous findings and affords a universal interpretation of ascending aorta mechanics in bicuspid aortopathy.
... Similar collagen levels were observed between control and ascending aneurysm samples [61,68,27], and between BAV and TAV phenotypes [104,103,27] contradicting the findings of significantly higher collagen in BAV compared with TAV and control [16]. Regardless, the organization of collagen may still be significantly changed during aneurysm development in the thoracic aorta [7]. ...
... Ferrara et al. [35] reported stronger and stiffer posterior regions with respect to anterior in the circumferential direction for thoracic aortic aneurysms, whereas the opposite trend was observed for the longitudinal direction. Kritharis et al. [68] found similar failure properties in the noncoronary sinuses of the control and aneurysm groups for both young and old patients, whereas failure stresses in the right and left coronary sinus regions were smaller circumferentially and greater longitudinally in aneurysms compared with control. ...
... In the study of Vande Geest et al. [150] no statistically significant gender-related differences were reported in terms of strength, unlike Sokolis & Iliopoulos [127] who identified that circumferential aneurysmatic specimens obtained from female patients exhibited significantly lower failure stresses compared with the ones obtained from male patients. Furthermore, failure stresses of the aorta are reported to decrease [92,39,68,36], and also the failure stretches [92,68,36] with increasing age. In general, strength was not correlated to diameter [28,55], but it was inversely related to wall thickness [140,28,55]. ...
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.
... The degenerative effects of ATAA formation on the mechanical properties of aortic wall are well recognized, but our group raised the question, several years ago, whether there is indeed a degenerative effect on wall strength. We reported [25] that ATAA is not associated with wall weakening, only with stiffening and reduced extensibility, and we made similar inferences for the contiguous aortic root aneurysms [26]. Our layer-specific data detailing nonsignificant differences in intimal and adventitial (albeit reduced medial) failure stress and reduced failure stretch of all layers in TAV-ATAA than in nonaneurysmal aorta support our previous observations while highlighting the weakened structural integrity of media in TAV-ATAA. ...
Background:
Previous studies have not examined the participation of intimal, medial, and adventitial layers in providing mechanical strength to the ascending thoracic aortic aneurysm (ATAA) wall compared to the non-aneurysmal aorta. A comparison is made herein of the mechanical properties of intact wall and its layers among ATAA and non-aneurysmal aorta, with explicit consideration of the effects of valve morphology, i.e. bicuspid (BAV) vs. tricuspid aortic valve (TAV), and aortic quadrant.
Methods:
Whole ATAA were taken from patients undergoing elective repair and non-aneurysmal aortas from age-matched autopsy subjects. These were cut into a couple of circumferential and longitudinal tissue strips for the intact wall and its layers per quadrant, permitting examination of the aortic wall as a multi-layered structure. Tissue was submitted to tensile-testing for determination of failure properties.
Results:
Intact wall and layer-specific failure stretches (i.e. extensibilities) were significantly greater in non-aneurysmal and BAV-ATAA than TAV-ATAA, unaccounted by elastin/collagen content changes. Intact wall failure stress (i.e. strength) was significantly greater in BAV-ATAA than TAV-ATAA, in analogy with medial failure stress. Failure stress and stretch associated negatively with age in most subject groups, layers, and intact wall, but failure stretch correlated positively with residual stretch (i.e. structural bonds between layers).
Conclusions:
No mechanical vulnerability of BAV-ATAA was found, corroborating current conservative guidelines regarding the management of bicuspid aortopathy. Weakening and added vulnerability was found in patients with valvular deficiency, aortic root aneurysm, hypertension, and hyperlipidemia. Aging led to increased susceptibility to dissection initiation and/or full rupture in both patient classes.
... The study by Kritharis and colleagues [1] represents a significant step toward this goal because it provides rare uniaxial failure stress measurements from 16 aneurysmal patients of different age (range, 19-82 years old), gender, risk factors, and comorbidities. Moreover, it characterizes aortic sinus tissue mechanical properties using a Fung-type model, which allows the anisotropic and nonlinear behavior of the aneurysmal and control sinus tissue (Fig 3) to be accurately simulated with only four material constants in each case ( Table 2). ...
Background
Although aneurysms of the ascending aorta and the aortic root are treated similarly in clinical guidelines, how biomechanical properties differ between these 2 segments of aorta is poorly defined.
Methods
Biomechanical testing was performed on tissue collected from the aortic root (normal = 11, aneurysm = 51) and the ascending aorta (normal = 21, aneurysm = 76). Energy loss, tangent modulus of elasticity, and delamination strength were evaluated. These biomechanical properties were then compared between (1) normal ascending and normal root tissue, (2) normal and aneurysmal root tissue, (3) normal and aneurysmal ascending tissue, and (4) aneurysmal root and aneurysmal ascending tissue. Propensity score matching was performed to further compare aneurysmal root and aneurysmal ascending aortic tissue. Clinical and biomechanical variables associated with decreased delamination strength in the aortic root were evaluated.
Results
The normal aortic root demonstrated greater viscoelastic behavior (energy loss 0.08 [0.06, 0.10] vs 0.05 [0.04, 0.06], P = .008), and greater resistance against delamination (93 [58, 126] mN/mm vs 54 [40, 63] mN/mm, P = .05) compared with the ascending aorta. Delamination strength was significantly reduced in aneurysms in both the root and the ascending aorta compared with their normal states. Aneurysms of the aortic root matched to the ascending aortic aneurysms in terms of baseline characteristics including size, were characterized by a larger decrease in delamination strength from baseline (Δ −59 mN/mm vs Δ −24 mN/mm). Aging (P = .003) and the presence of hypertension (P = .02) were associated with weakening of the aortic root, while diameter did not have this association (P = .29).
Conclusions
The normal aortic root was found to have distinct biomechanical properties compared with the ascending aorta. When aneurysms form in the aortic root, there is less strength against delamination, without other biomechanical changes such as increased energy loss observed in aneurysmal ascending aortas. Age and hypertension were associated decreased aortic wall strength in the aortic root, whereas diameter had no such association.
Objectives
We hypothesized that tissue characteristics vary significantly along zone zero, which may be reflected by regional differences in stored elastic energy. Our objectives were to (1) characterize the regional variation in stored elastic energy within tissues of the aortic zone zero, and (2) identify the association between this variation and patient characteristics.
Methods
From 2/2018 to 1/2021, 123 aortic tissue samples were obtained from the aortic root, proximal, and distal ascending aorta of 65 adults undergoing elective ascending aorta replacement. Biaxial biomechanics testing was performed to obtain tissue elastic energy at inflection point and compared to patient demographics and pre-operative computed tomography imaging. Coefficient models were fit using B-spline to interrogate the relationship between elastic energy, region, and patient characteristics.
Results
Mean elastic energy at inflection point was 24.3±15.6 kJ/m³. Elastic energy increased significantly between the root and proximal, and root and distal ascending aorta and decreased with increasing age. Differences due to history of connective tissue disorder (CTD) and bicuspid aortic valve (BAV) were significant but diminished when controlled for other patient characteristics. Among covariates, age and region were found to be the most important predictors for elastic energy.
Conclusions
Aortic tissue biomechanical metrics varied across regions and with patient characteristics within the aortic zone zero. Assessment of endovascular outcomes in the ascending aorta must closely consider the region of deployment and variable tissue qualities along the length of the landing zone. Regional variation in tissue characteristics should be incorporated into existing patient-specific models of aortic mechanics.
Purpose
Aortic dissection (AD) is a life-threatening event that occurs when the intimal entry tear propagates and separates inner from outer layers of the aorta. Diameter, the current criterion for aneurysm repair, is far from ideal and additional evidence to optimize clinical decision would be extremely beneficial. Biomechanical investigation of the regional failure properties of aortic tissue is essential to understand and proactively prevent AD. We previously studied biaxial mechanical properties of healthy human aorta. In this study, we investigated the regional failure properties of healthy human ascending aorta (AscAo) including sinuses of Valsalva (SOV), and sinotubular junction (STJ).
Results
A total of 430 intact tissue samples were harvested from 19 healthy donors whose hearts were excluded from heart transplantation. The donors had mean age of 51 ± 11.7 years and nearly equal gender distribution. Samples were excised from aortic regions and subregions at defined locations. Tissue strips were subjected to either biaxial or uniaxial failure testing. Wall thickness varied regionally being thickest at AscAo (2.08 ± 0.66 mm) and thinnest at SOV (1.46 ± 0.31 mm). Biaxial testing demonstrated hyperplastic behavior of aortic tissues. Posterior and lateral STJ subregions were found to be stiffer than anterior and medial subregions in both circumferential and longitudinal directions. Failure stresses were significantly higher in the circumferential than longitudinal directions in each subregion of AscAo, STJ, and SOV. Longitudinal failure stresses were significantly greater in AscAo than those in STJ or SOV. Longitudinal failure stresses in AscAo were much smaller anteriorly than posteriorly, and medially than laterally.
Conclusions
The finding of weakest region at the sinotubular junction along the longitudinal direction corroborates clinical observations of that region being commonly involved as the initial site of intimal tear in aortic dissections. Failure stretch ratios correlated to elastic modulus at each region. Furthermore, strong correlation was seen between STJ failure stresses and elastic modulus at physiological pressure along both circumferential and longitudinal directions. Correlating in-vivo aortic elastic modulus based on in-vivo imaging with experimentally determined elastic modulus at physiological pressure and failure stresses may potentially provide valuable information regarding aortic wall strength. Better understanding of aortic biomechanics in normal physiologic and aneurysmal pathologic states may aid in determining risk factors for predicting dissection in patient-specific fashion.
Mechanical properties and microstructural modifications of vessel tissues are strongly linked, as established in the state of the art of cardiovascular diseases. Techniques to obtain both mechanical and structural information are reported, but the possibility to obtain real-time microstructural and macrostructural data correlated is still lacking. An experimental approach to characterize the aortic tissue is presented. A setup integrating biaxial traction and Small Angle Light Scattering (SALS) analysis is described. The system was adopted to test ex-vivo aorta specimens from healthy and aneusymatic (aTAA) cases. A significant variation of the fiber dispersion with respect to the unloaded state was encountered during the material traction. The corresponding microstructural and mechanical data were successfully used to fit a given anisotropic constitutive model, with satisfactory R2 values (0.97±0.11 and 0.96±0.17, for aTAA and healthy population, respectively) and fiber dispersion parameters variations between the aTAA and healthy populations (0.39±0.23 and 0.15±0.10). The method integrating the biaxial/SALS technique was validated, allowing for real-time synchronization between mechanical and microstructural analysis of anisotropic biological tissues.
A thorough understanding of the aortic root structure and biomechanics is necessary when performing aortic valve-sparing procedures in patients with aortic root aneurysms. This study aimed to evaluate the amount of collagen and biomechanics at different levels and segments of the aortic root. Ten aortic roots from healthy pigs were excised including the aortic annulus, the sinuses of Valsalva, and the sinotubular junction (STJ). Specimens were further divided into three circumferential segments; left sinus (LC), right sinus (RC), and non-coronary (NC) sinus. Collagen was determined using hydroxyproline analysis and specimens were tested biomechanically for stress-strain relations. The annulus showed significantly larger average maximum stiffness (9.6±4.5N/mm) compared with the sinus (4.5±2.0N/mm) and STJ (4.8±1.8N/mm). The average collagen content was likewise higher in the annulus (4.0±1.0mg/ml) compared with the sinus (2.4±0.6mg/ml) and STJ (2.2±0.5mg/ml) for all three segments. The NC sinus segment exhibited a significantly larger maximum stiffness and stress under static conditions compared with the RC. These results suggest that the aortic root is heterogeneous in both structure and biomechanical properties and that it varies both in levels and segments of the aortic root. Future surgical approaches should consider enhanced strength parameters for specific areas of the aortic root to achieve the best results when performing aortic valve-sparing techniques. From this study, we conclude that the aortic annulus needs special attention to imitate normal physiologic properties during aortic valve-sparing surgery due to its higher maximum stiffness, stress, and load. Modified future surgical procedures could potentially prevent recurrent aneurysmal formation.
