Influence of atherosclerosis on anisotropy and incompressibility of the human thoracic aortic wall

• Autorzy: Kozun Marta , Chwilkowska Agnieszka , Pezowicz Celina , Kobielarz Magdalena

Identyfikatory

DOI

10.1016/j.bbe.2020.11.004

• Języki publikacji: EN

Abstrakty

EN

In this study, we analysed the influence of atherosclerosis on the anisotropic and incompressible behaviour of the human thoracic aortic wall under mechanical loads. The mechanical tests involved preparations of the human thoracic aortic wall, which were evaluated based on the six-stage histological classification of atherosclerosis proposed by Stary. Anisotropy was evaluated on the basis of directional tests of mechanical properties, which were determined based on a uniaxial tensile test conducted in two directions, i.e. longitudinal and circumferential. The evaluation of incompressibility was carried out based on the product of the stretch ratios obtained in the x–y and y–z planes and on the basis of Poisson's ratio. The results presented in this study indicate that the blood vessel wall is an anisotropic material only in the case of normal vessels and in early atherosclerotic lesions. Atherosclerosis progression causes a gradual loss of the anisotropic character of the work of the thoracic aortic wall in moderate and very advanced stages of atherosclerosis under mechanical loads. The results show that the wall of the thoracic aorta is an incompressible material. Development of atherosclerosis does not cause a loss of incompressibility of the thoracic aorta. This study is the only one so far that presents changes in the mechanical properties at all stages of atherosclerotic development. A large number of preparations were included in the study, which is important for the results obtained due to the multi-factorial etiology of atherosclerosis development.

Słowa kluczowe

EN

human cardiovascular system; cardiovascular disease; atherosclerosis; anisotropy; incompressibility

PL

układ sercowo-naczyniowy; choroba układu krążenia; miażdżyca; anizotropia

• Wydawca: Nałęcz Institute of Biocybernetics and Biomedical Engineering of the Polish Academy of Sciences ; Elsevier
• Czasopismo: Biocybernetics and Biomedical Engineering
• Rocznik: 2021
• Tom: Vol. 41, no. 1
• Strony: 15--27
• Opis fizyczny: Bibliogr. 72 poz., rys., tab., wykr.

Twórcy

autor

Kozun Marta

• Wroclaw University of Science and Technology, Faculty of Mechanical Engineering, Department of Biomedical Engineering, Mechatronics and Theory of Mechanism, Wroclaw, Poland

autor

Chwilkowska Agnieszka

• Wroclaw Medical University, Department of Medical Biochemistry, Wroclaw, Poland

autor

Pezowicz Celina

• Wroclaw University of Science and Technology, Faculty of Mechanical Engineering, Department of Mechanics, Materials and Biomedical Engineering, Wroclaw, Poland

autor

Kobielarz Magdalena

• Wroclaw University of Science and Technology, Faculty of Mechanical Engineering, Department of Mechanics, Materials and Biomedical Engineering, Wroclaw, Poland

Bibliografia

• [1] Vito R, Dixon S. Blood vessel constitutive models—1995- 2002. Annu Rev Biomed Eng 2003;5:413–39.
• [2] Chuong CJ, Fung YC. On residual stress in arteries. J Biomech Eng 1986;108(2):189–92.
• [3] Eelkema R, Cowin P. General themes in cell-cell junctions and cell adhesion. Tight Junctions 2001;121.
• [4] Carew TE, Vaishnav RN, Patel DJ. Compressibility of the arterial wall. J Am Heart Assoc 1968;23:61–8.
• [5] Holzapfel GA, Ogden RW. Biomechanics of soft tissue in cardiovascular systems. Wien New York: Springer-Verlag; 2003.
• [6] Lawton RW. The thermoelastic behavior of isolated aortic strip of the dog. Circ Res 1954;2(344).
• [7] Dobrin PB, Rovick AA. Influence of vascular smooth muscle on contractile mechanics and elasticity of arteries. Am J Physiol 1969;217(6):1644–51.
• [8] Karimi A, Sera T, Kudo S, Navidbakhsh M. Experimental verification of the healthy and atherosclerotic coronary arteries incompressibility via Digital Image Correlation. Artery Res 2016;16:1–7.
• [9] Jiu-sheng R. Effects of dispersion of fiber orientation on the mechanical property of the arterial wall. J Theor Biol 2012;21(301):153–60.
• [10] Kozun M, Kobielarz M, Chwilkowska A, Pezowicz C. The impact of development of atherosclerosis on delamination resistance of the thoracic aortic wall. J Mech Behav Biomed Mater 2018;79:292–300.
• [11] Liu H, Zhang M, Liu M, Martin C, Cai Z, Sun W. Finite element simulation of three dimensional residual stress in the aortic wall using an anisotropic tissue growth model. Journal of the Mechanical Behaviour of Biomedical 2019;92:188–96.
• [12] Waffenschmidt T, Menzel A. Extremal states of energy of a double-layered thick-walled tube-application to residually stressed arteries. J Mech Behav Biomed Mater 2014;635–54.
• [13] Weizsacker HW, Pinto JG. Isotropy and anisotropy of the arterial wall. J Biomech 1988;21(6):477–87.
• [14] Patel DJ, Fry DL. The elastic symmetry of arterial segments in dogs. Circ Res 1969;24(1):1–8.
• [15] Wegenseil JE, Mechami RP. Elastin in large artery stiffness and hypertension. J Cardiovasc Transl Res 2012;5(3):264–73.
• [16] Cardamone L, Velentin A, Eberth JF, Humphrey JD. Origin of axial prestretch and residual stress in arteries. Biomech Model Mechanobiol 2009;8(6):431–46.
• [17] Snowhill PB, Silver FH. A mechanical model of porcine vascular tissues-Part II: stress-strain and mechanical properties of juvenile porcine blood vessels. Cardiovascular Engineering 2005;5:157–69.
• [18] Rezakhaniha R, Fonck E, Genoud C, Stergiopulos N. Role of elastin anisotropy in structural strain energy functions of arterial tissue. Biomechanical Modelling of Mechanobiology 2011;10:599–611.
• [19] Sigaeva T, Sommer G, Holzapfel AA, Di Martino ES. Anisotropic residual stresses in arteries. J R Soc Interface 2019;16:1–12.
• [20] Sherifova S, Holzapfek GA. Biomechanics of aortic wall failure with a focus on dissection and aneurysm: a review. Acta Biomater 2019;99:1–17.
• [21] Pejcic S, Hassan SMA, Rival DE, Bisleri G. Characterizing the mechanical properties of the aortic wall. Vessel Plus 2019;32(3).
• [22] Iliopoulos DC, Deveja RP, Kritharis EP, Perrea D, Sionis GD, Toutouzas K, et al. Regional and directional variations in the mechanical properties of ascending thoracic aortic aneurysm. Med Eng Phys 2009;31:1–9.
• [23] Liu M, Liang L, Sulejmani F, Lou X, Iannucci G, Chen E, et al. Identification of in vivo nonlinear anisotropic mechanical properties of ascending thoracic aortic aneurysm from patient-specific CT scans. Sci Rep 2019;9:12983.
• [24] Niestrawska JA, Regitnig P, Viertler Ch, Cohnert TU, Babu AR, Holzapfel GA. The role of tissue remodelling in mechanics and pathogenesis of abdominal aortic aneurysms. Acta Biomater 2019;88:149–61.
• [25] O'Leary SA, Kavanagh EG, Grace PA, McGloughlin TM, Doyle BJ. The biaxial mechanical behaviour of abdominal aortic aneurysm intraluminal thrombus: classification of morphology and the determination of layer and region specific properties. J Biomech 2014;47:1430–7.
• [26] Sassani SG, Kakisis J, Tsangaris S, Sokolis DP. Layer-dependent wall properties of abdominal aortic aneurysms: experimental study and material characterization. Journal of the Mechanical Behaviour of Biomedical 2015;49:141–61.
• [27] Schriefl AJ, Zeindlinger G, pierce DM, Regitnig P, Holzapfel GA. Determination of the layer-specific distributed collagen fiber orientations in human thoracic and abdominal aortas and common iliac arteries. J R Soc Interface 2012;9:1275–86.
• [28] Thubikar MJ, Labrosse M, Robicsek J, Al-Soudi J, Fowler B. Mechanical properties of abdominal aortic aneurysm wall. J Med Eng Technol 2001;25:133–42.
• [29] Trabelsi O, Duphrey A, Favre J-P-P, Avril S. Predictive models with patient specific material properties for the biomechanical behavior of ascending thoracic aneurysm,. Ann Biomed Eng 2016;44:84–98.
• [30] Vande Geest JP, Sacks MS, Vorp DA. The effects of aneurysm on the biaxial mechanical behaviour of human abdominal aorta. J Biomech 2006;39:1324–34.
• [31] Raghavan ML, Webster MW, Vorp DA. Ex vivo biomechanical behavior of abdominal aortic aneurysm: assessment using a new mathematical model. Ann Biomed Eng 1996;24(5):573–82.
• [32] Sommer G, Sherifova S, Oberwalder PJ, Dapunt OE, Ursomanno PA, DeAnda A, et al. Mechanical strength of aneurysmatic and dissected human thoracic aortas at different shear loading modes. J Biomech 2016;49:2374–82.
• [33] Vorp DA, Schiro BJ, Ehrlich MP, Juvonen TS, Ergin MA, Griffith BP. Effect of aneurysm on the tensile strength and biomechanical behaviour of the ascending thoracic aorta. Ann Thorac Surg 2003;800:1210–4.
• [34] Chung J, Lachapelle E, Wener R, Cartier B, De Varennes R, Fraser RL. Energy loss, a novel biomechanical parameter, correlates with aortic aneurysm size and histopathologic findings. J Thorac Cardiovasc Surg 2014;148:1082–9.
• [35] Chung J, Lachapelle R, Cartier R, Mongrain RL. Loss of mechanical directional dependency of the ascending aorta with severe medial degeneration. Cardiovasc Pathol 2017;26:45–50.
• [36] Holzapfel GA, Sommer G, Regitnig P. Anisotropic mechanical properties of tissues components in human atherosclerotic plaques. J Biomech Eng 2004;126:657–65.
• [37] Teng Z, Zhang Y, Huang Y, Feng J, Yuan J, Lu Q, et al. Material properties of components in human carotid atherosclerotic plaques: a uniaxial extension study. Acta Biomater 2014;10:5055–63.
• [38] Karimi A, Navidbakhsh M, Shojaei A, Faghihi S. Measurement of the uniaxial mechanical properties of healthy and atherosclerotic human coronary arteries. Mater Sci Eng 2013;33:2550–4.
• [39] Geest MJ, Sacks D. Vorp, Age dependency of the biaxial biomechanical behaviour of human abdominal aorta. J Biomech Eng 2004;126:815–22.
• [40] Holzapfel G, Weizsacker H. Biomechanical behavior of the arterial wall and its numerical characterization. Comput Biol Med 1998;28:377–92.
• [41] Witzenburg CM, Dhume RY, Shah SB, Korenczuk CE, Wagner HP, Alford PW, et al. Failure of the porcine ascending aorta: multidirectional experiments and a unifying microstructural model. J Biomech Eng 2017;139:1–14.
• [42] Legerer Ch, Almsherqi ZA, Dokos S, McLachlan CS. Computational evaluation of an extra-aortic elastic-wrap applied to simulated aging anisotropic human aorta models. Sci Rep 2019;9:20109.
• [43] Akyildiz AC, Speelman L, Gijsen FJH. Mechanical properties of human atherosclerotic intima tissue. J Biomech 2014;47:773–83.
• [44] Kot M, Kobielarz M, Maksymowicz K. Assessment of mechanical properties of arterial calcium deposition. Trans Famena 2011;35(3):49–56.
• [45] Stary HC, Blankenhorn DH, Chandler AB, Glagov S, Insull Jr W, Richardson M, et al. A definition of the intima of human arteries and of its atherosclerosis-prone regions. Arterioscler Thromb Vasc Biol 1992;12:120–34.
• [46] Stary HC, Chandler AB, Glagov S, Guyton JR, Insull Jr W, Rosenfeld ME, et al. A definition of initial, fatty streak, and intermediate lesions of atherosclerosis. Arterioscler Thromb Vasc Biol 1994;14:840–56.
• [47] Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W, et al. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. Arterioscler Thromb Vasc Biol 1995;15:1512–31.
• [48] Stary HC. Natural history and histological classification of atherosclerotic lesions: an update. Arterioscler Thromb Vasc Biol 2000;20:1177–8.
• [49] Hoshino T, Chow LA, Hsu JJ, Perlowski AA, Abedin M, Tobis J, et al. Mechanical stress analysis of a rigid inclusion in distensible material; a model of atherosclerotic calcification and plaque vulnerability, American Journal of Physiology. Heart and Circulatory Physiology 2009;297(2):802–10.
• [50] Imoto K, Hiro T, Fujii T, Murashige A, Fukumoto Y, Hashimoto G, et al. Longitudinal structural determinants of atherosclerotic plaque vulnerability: a computational analysis of stress distribution using vessel models and three-dimensional intravascular ultrasound imaging. J Am Coll Cardiol 2005;46(8):1507–15.
• [51] Vengrenyuk Y, Cardoso L, Weinbaum S. Micro-CT based analysis of a new paradigm for vulnerable plaque rupture: cellular microcalcifications in fibrous caps. Mol Cell Biomech 2008;5(1):37–47.
• [52] Cardoso L, Weinbaum S. Changing views of the biomechanics of vulnerable plaque rupture: a review. Ann Biomed Eng 2014;42(2):415–31.
• [53] Barrett HE, van der Heiden K, Farrell E, Gijsen FJH, Akyildiz AC. Calcifications in atherosclerotic plaques and impact on plaque biomechanics. J Biomech 2019;87:1–12.
• [54] Stary HC. Natural history of calcium deposits in atherosclerosis progression and regression. Cardiol J 2000;89(Suppl 2). II/28-II/35.
• [55] Stary HC. Atlas of atherosclerosis progression and regression, 2nd edition on CD-ROM. Parthenon Publishing Group; 2004.
• [56] Kuzan A, Chwilkowska A, Pezowicz C, Witkiewicz W, Gamian A, Maksymowicz K, et al. The content of collagen type II in human arteries is correlated with stage of atherosclerosis and calcification foci. Cardiovasc Pathol 2017;28:21–7.
• [57] Weisbecker H, Pierce DM, Regitnig P, Holzapfel GA. Layer-specific damage experiments and modeling of human thoracic and abdominal aortas with non-atherosclerotic intimal thickening. J Mech Behav Biomed Mater 2012;12:93–106.
• [58] Liu Y, Zhang W, Wang C, Kassab GS. A linearized and incompressible constitutive model for arteries. J Theor Biol 2011;286(1):85–91.
• [59] Choudhury N, Bouchot O, Rouleau L, Tremblay D, Cartier R, Butany J, et al. Local mechanical and structural properties of healthy and diseased human ascending aorta tissue. Cardiovasc Pathol 2009;18(2):83–91.
• [60] Duprey A, Khanafer K, Schlicht M, Avril S, Williams D, Berguer R. In vitro characterization of physiological and maximum elastic modulus of ascending thoracic aortic aneurysm using uniaxial tensile testing. Eur J Vasc Endovasc Surg 2010;39:700–7.
• [61] Teng Z, Tang D, Zheng J, Woodard PK, Hoffman AH. An experimental study on ultimate strength of the adventitia and media of human atherosclerotic arteries in circumferential and axial directions. J Biomech 2009;42:2535–9.
• [62] Karimi A, Navidbakhsh M, Shojaei A. A combination of histological analyses and uniaxial tensile tests to determine the material coefficient of the healthy and atherosclerotic human coronary arteries. Tissue Cell 2015;47(2):152–8.
• [63] Leopold JA. Vascular calcification: mechanisms of vascular smooth muscle cell calcification. Trends Cardiovasc Med 2015;25:267–74.
• [64] Proudfoot D, Shanahan C. Biology of calcification in vascular cells: intima versus media. Herz 2001;26:245–51.
• [65] Ewence A, Bootman M, Roderick H, Skepper J, McCarthy G, Epple M, et al. Calcium phosphate crystals induce cell death in human vascular smooth muscle cells: a potential mechanism in atherosclerotic plaque destabilization. Circ Res 2008;103:e28–34.
• [66] Kobielarz M, Kozun M, Gasior-Glogowska M, Chwilkowska A. Mechanical and structural properties of different types of human aortic atherosclerotic plaques. J Mech Behav Biomed Mater 2020;109103837.
• [67] Cahalane RM, Walsh MT. Nanoindentation of calcified and non-calcified components of atherosclerotic tissues. Exp Mech 2020. http://dx.doi.org/10.1007/s11340-020-00635-z.
• [68] Barrett SRH, Sutcliffe MPF, Howarth S, Li ZY, Gillard JH. Experimental measurement of the mechanical properties of carotid atherothrombotic plaque fibrous cap, 2009. Journal of Biomechanics 2009;42:1650–5.
• [69] Chai C, Speelman L, Oomens C, Baaijens F. Compressive mechanical properties of atherosclerotic plaques-indentation test to characterise the local anisotropic behaviour. J Biomech 2014;47:784–92.
• [70] Cahalane RM, Barretta HE, O'Brien JM, Kavanagh EG, Moloney MA, .Walsh MT. Relating the mechanical properties of atherosclerotic calcification to radiographic density: a nanoindentation approach. Acta Biomater 2018;80:228–36.
• [71] Polak-Krasna K, Robak-Nawrocka S, Szotek S, Czyz M, Gheek D, Pezowicz C. The denticulate ligament – tensile characterisation and finite element micro-scale model of the structure stabilising spinal cord. J Mech Behav Biomed Mater 2019;91:10–7.
• [72] Wysocki M, Kobus K, Szotek S, Kobielarz M, Kuropka P, Bedzinski R. Biomechanical effect of rapid mucoperiosteal palatal tissue expansion with the use of osmotic expanders. J Biomech 2011;44(7):1313–20.

Uwagi

Opracowanie rekordu ze środków MNiSW, umowa Nr 461252 w ramach programu "Społeczna odpowiedzialność nauki" - moduł: Popularyzacja nauki i promocja sportu (2021).