Linking Aortic Mechanical Properties, Gene Expression and Microstructure: A New Perspective on Regional Weakening in Abdominal Aortic Aneurysms

Forneris, Arianna; Kennard, Jacob; Ismaguilova, Alina; Shepherd, Robert D.; Studer, Deborah; Bromley, Amy; Moore, Randy D.; Rinker, Kristina D.; Martino, Elena S. Di

doi:10.3389/fcvm.2021.631790

Cited by 8 publications

(14 citation statements)

References 39 publications

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“…Because of the tissue's response to site-specific hemodynamic conditions, the aortic wall presents highly heterogeneous material properties, especially in the presence of degenerative processes. The effect of wall-shear stress has been linked to disease progression before, with literature reporting on its role in thrombus formation and accumulation-likely leading to hypoxia and further loss in tissue integrity, as well as aneurysm rupture [2,[4][5][6][7]. The present findings, in agreement with previous literature, highlight the aneurysm as a region of significantly disturbed flow where further degeneration of the tissue is likely to occur.…”

Section: Discussionsupporting

confidence: 90%

“…The CFD commercial software Fluent (version 2019.2; Ansys, Canonsburg, PA, USA) was used to run transient-time simulations and reproduce the aortic fluid dynamics during a cardiac cycle. A semi-implicit method for pressure-linked equations (SIMPLE algorithm) was employed to couple pressure and velocity and solve the Navier-Stokes equations for the blood modelled as an incompressible, Newtonian fluid undergoing laminar flow [4,5]. A second order upwind formulation and a second order implicit transient formulation were used for spatial and temporal discretization respectively.…”

Section: Wall Shear Stressmentioning

confidence: 99%

“…In recent years, different studies highlighted the inadequacy of the diameter criterion by pointing out the high level of heterogeneity in the aneurysmal tissue and its impact on the risk of rupture of individual aortas [1][2][3][4][5]. Aneurysm initiation and progression are multifactorial processes linked to the tissue's heterogeneous remodeling and structural degradation in response to the local environment, including both mechanical (altered hemodynamics) and biological factors (inflammation, presence of intraluminal thrombus) [6][7][8].…”

Section: Introductionmentioning

confidence: 99%

“…Equally important is the need to obtain non-invasive means to access information on the state of individual aortas. To this effect, there have been several efforts to model the biomechanics of AAAs, both fluid and solid, that have led to so-called biomechanicsbased indices as a surrogate measure to estimate growth and rupture risk [4,5,22,23]. The heterogeneity along the length and circumference of the aorta should be incorporated in these parameters.…”

Section: Introductionmentioning

confidence: 99%

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Heterogeneity of Ex Vivo and In Vivo Properties along the Length of the Abdominal Aortic Aneurysm

et al. 2021

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The current clinical guidelines for the management of aortic abdominal aneurysms (AAAs) overlook the structural and mechanical heterogeneity of the aortic tissue and its role in the regional weakening that drives disease progression. This study is a comprehensive investigation of the structural and biomechanical heterogeneity of AAA tissue along the length and circumference of the aorta, by means of regional ex vivo and in vivo properties. Biaxial testing and histological analysis were performed on ex vivo human aortic specimens systematically collected during open repair surgery. Wall-shear stress and three-dimensional principal strain analysis were performed to allow for in vivo regional characterization of individual aortas. A marked effect of position along the aortic length was observed in both ex vivo and in vivo properties, with the central regions corresponding to the aneurysmal sac being significantly different from the adjacent regions. The heterogeneity along the circumference of the aorta was reflected in the ex vivo biaxial response at low strains and histological properties. Present findings uniquely show the importance of regional characterization for aortic assessment and the need to correlate heterogeneity at the tissue level with non-invasive measurements aimed at improving clinical outcomes.

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Section: Discussionsupporting

confidence: 90%

Section: Wall Shear Stressmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Heterogeneity of Ex Vivo and In Vivo Properties along the Length of the Abdominal Aortic Aneurysm

et al. 2021

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“…Eventually, this could help contribute to better informed clinical decision making on elective aneurysm elimination by open surgery or endovascular treatment. Thus in recent years several groups have proposed the use of in vivo full field strain imaging for gathering additional patient-specific information on degenerative changes and disease progress beyond the maximum diameter criterion (Bersi et al, 2016;Cebull et al, 2019;Derwich et al, 2016Derwich et al, , 2020Forneris et al, 2020Forneris et al, , 2021Karatolios et al, 2013;Satriano et al, 2015;Wittek et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Biomechanical Characterization of Tissue Types in Murine Dissecting Aneurysms based on Histology and 4DUltrasound-Derived Strain

Hegner

Cebull²,

Gámez

et al. 2023

Preprint

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Abdominal aortic aneurysm disease is the local enlargement of the aorta, typically in the infrarenal section, causing up to 200,000 deaths/year. In vivo information to characterize the individual elastic properties of the aneurysm wall in terms of rupture risk is lacking. We used a method that combines 4D ultrasound and direct deformation estimation to compute in vivo 3D Green-Lagrange strain in murine angiotensin II-induced dissecting aortic aneurysms, a commonly used mouse model. After euthanasia, histological staining of cross-sectional sections along the aorta was performed in areas where in vivo strains had previously been measured. The histological sections were segmented into intact and fragmented elastin, thrombus with and without red blood cells, and outer vessel wall including the adventitia. Meshes were then created from the individual contours based on the histological segmentations. The isolated contours of the outer wall and lumen from both imaging modalities were registered individually using a coherent point drift algorithm. 2D finite element models were generated from the meshes, and the displacements from the registration were used as displacement boundaries of the lumen and wall contours. Based on the resulting deformed contours, the strains recorded were grouped according to segmented tissue regions. Strains were highest in areas containing intact elastin without thrombus attachment. Strains in areas with intact elastin and thrombus attachment, as well as areas with disrupted elastin, were significantly lower. Strains in thrombus regions with red blood cells were significantly higher compared to thrombus regions without. We then compared this analysis to statistical distribution indices and found that the results of each aligned, elucidating the relationship between vessel strain and structural changes. This work demonstrates the possibility of advancing in vivo assessments to a micro-structural level ultimately improving patient outcomes.

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Biomechanical characterization of tissue types in murine dissecting aneurysms based on histology and 4D ultrasound-derived strain

Hegner,

Cebull,

Gámez

et al. 2023

Biomech Model Mechanobiol

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Abdominal aortic aneurysm disease is the local enlargement of the aorta, typically in the infrarenal section, causing up to 200,000 deaths/year. In vivo information to characterize the individual elastic properties of the aneurysm wall in terms of rupture risk is lacking. We used a method that combines 4D ultrasound and direct deformation estimation to compute in vivo 3D Green-Lagrange strain in murine angiotensin II-induced dissecting aortic aneurysms, a commonly used mouse model. After euthanasia, histological staining of cross-sectional sections along the aorta was performed in areas where in vivo strains had previously been measured. The histological sections were segmented into intact and fragmented elastin, thrombus with and without red blood cells, and outer vessel wall including the adventitia. Meshes were then created from the individual contours based on the histological segmentations. The isolated contours of the outer wall and lumen from both imaging modalities were registered individually using a coherent point drift algorithm. 2D finite element models were generated from the meshes, and the displacements from the registration were used as displacement boundaries of the lumen and wall contours. Based on the resulting deformed contours, the strains recorded were grouped according to segmented tissue regions. Strains were highest in areas containing intact elastin without thrombus attachment. Strains in areas with intact elastin and thrombus attachment, as well as areas with disrupted elastin, were significantly lower. Strains in thrombus regions with red blood cells were significantly higher compared to thrombus regions without. We then compared this analysis to statistical distribution indices and found that the results of each aligned, elucidating the relationship between vessel strain and structural changes. This work demonstrates the possibility of advancing in vivo assessments to a microstructural level ultimately improving patient outcomes.

show abstract

Linking Aortic Mechanical Properties, Gene Expression and Microstructure: A New Perspective on Regional Weakening in Abdominal Aortic Aneurysms

Cited by 8 publications

References 39 publications

Heterogeneity of Ex Vivo and In Vivo Properties along the Length of the Abdominal Aortic Aneurysm

Heterogeneity of Ex Vivo and In Vivo Properties along the Length of the Abdominal Aortic Aneurysm

Biomechanical Characterization of Tissue Types in Murine Dissecting Aneurysms based on Histology and 4DUltrasound-Derived Strain

Biomechanical characterization of tissue types in murine dissecting aneurysms based on histology and 4D ultrasound-derived strain

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