Abstract
Mounting evidence suggests that the pulsatile character of blood pressure and flow within large arteries plays a particularly important role as a mechano-biological stimulus for wall growth and remodeling. Nevertheless, understanding better the highly coupled interactions between evolving wall geometry, structure, and properties and the hemodynamics will require significantly more experimental data. Computational fluid–solid-growth models promise to aid in the design and interpretation of such experiments and to identify candidate mechanobiological mechanisms for the observed arterial adaptations. Motivated by recent aortic coarctation models in animals, we used a computational fluid–solid interaction model to study possible local and systemic effects on the hemodynamics within the thoracic aorta and coronary, carotid, and cerebral arteries due to a distal aortic coarctation and subsequent spatial variations in wall adaptation. In particular, we studied an initial stage of acute cardiac compensation (i.e., maintenance of cardiac output) followed by early arterial wall remodeling (i.e., spatially varying wall thickening and stiffening). Results suggested, for example, that while coarctation increased both the mean and pulse pressure in the proximal vessels, the locations nearest to the coarctation experienced the greatest changes in pulse pressure. In addition, after introducing a spatially varying wall adaptation, pressure, left ventricular work, and wave speed all increased. Finally, vessel wall strain similarly experienced spatial variations consistent with the degree of vascular wall adaptation.
Similar content being viewed by others
References
Aguirre-Sanceledonio M, Fossum TW, Miller MW, Humphrey JD, Berridge BR, Herraez P (2003) Collateral circulation in experimental coarctation of the aorta in minipigs: a possible association with hypertrophied vasa vasorum. J Comp Pathol 128: 165–171
Arribas SM, Hinek A, González MC (2006) Elastic fibres and vascular structure in hypertension. Pharmacol Ther 111(3): 771–791
Balossino R, Pennati G, Migliavacca F, Formaggia L, Veneziani A, Tuveri M, Dubini G (2009) Computational models to predict stenosis growth in carotid arteries: which is the role of boundary conditions?. Comput Methods Biomech Biomed Eng 12(1): 113–123
Baretta A, Corsini C, Yang W, Vignon-Clementel IE, Marsden AL, Feinstein JA, Hsia TY, Dubini G, Migliavacca F, Pennati G (2011) Virtual surgeries in patients with congenital heart disease: a multi-scale modelling test case. Philos Trans R Soc A 369: 4316–4330
Bazilevs Y, Hsu MC, Benson DJ, Sankaran S, Marsden AL (2009) Computational fluid-structure interaction: methods and application to a total cavopulmonary connection. Comput Mech 45: 77–89
Bazilevs Y, Gohean JR, Hughes TJR, Moser RD, Zhang Y (2009) Patient-specific isogeometric fluid-structure interaction analysis of thoracic aortic blood flow due to implantation of the Jarvik 2000 left ventricular assist device. Comput Methods Appl Mech Eng 198(45–46): 3534–3550
Chien S, Li S, Shyy YJ (1998) Effects of mechanical forces on signal transduction and gene expression in endothelial cells. Hypertension 31(1 Pt 2): 162–169
Choi G, Cheng CP, Wilson NM, Taylor CA (2008) Methods for quantifying three-dimensional deformation of arteries due to pulsatile and non-pulsatile forces: implications for the design of stents and stent grafts. Ann Biomed Eng 37(1): 14–33
Coogan JS, Chan FP, Taylor CA, Feinstein JA (2011) Computational fluid dynamic simulations of aortic coarctation comparing the effects of surgical- and stent-based treatments on aortic compliance and ventricular workload. Catheter Cardiovasc Interv 77(5): 680–691
Dajnowiec D, Langille BL (2007) Arterial adaptations to chronic changes in haemodynamic function: coupling vasomotor tone to structural remodelling. Clin Sci (Lond) 113(1): 15–23
Dart AM, Kingwell BA (2001) Pulse pressure—a review of mechanisms and clinical relevance. J Am Coll Cardiol 37(4): 975–984
de Korte CL, Carlier SG, Mastik F, Doyley MM, van der Steen AFW, Serruys PW, Bom N (2002) Morphological and mechanical information of coronary arteries obtained with intravascular elastography. Eur Heart J 23: 405–413
Eberth JF, Gresham VC, Reddy AK, Popovic N, Wilson E, Humphrey JD (2009) Importance of pulsatility in hypertensive carotid artery growth and remodeling. J Hypertens 27(10): 2010–2021
Eberth JF, Popovic N, Gresham VC, Wilson E, Humphrey JD (2010) Time course of carotid artery growth and remodeling in response to altered pulsatility. Am J Physiol Heart Circ Physiol 299(6): H1875–H1883
Figueroa C, Baek S, Taylor C, Humphrey J (2009) A computational framework for coupled solid-fluid-growth mechanics in cardiovascular simulations. Comput Methods Appl Mech Eng 198: 3583–3602
Figueroa CA, Vignon-Clementel IE, Jansen KC, Hughes TJ, Taylor CA (2006) A coupled momentum method for modeling blood flow in three-dimensional deformable arteries. Comput Methods Appl Mech Eng 195: 5685–5706
Gibbons GH, Dzau VJ (1994) The emerging concept of vascular remodeling. N Engl J Med 330(20): 1431–1438
Giddens DP, Mabon RF, Cassanova RA (1976) Measurements of disordered flows distal to subtotal vascular stenosis in the thoracic aortas of dogs. Circ Res 39: 112–119
Gow BS, Hadfield CD (1979) The elasticity of canine and human coronary arteries with reference to postmortem changes. Circ Res 45(5): 588–594
Guyton AC, Hall JE (2006) Textbook of medical physiology. Saunders, Philadelphia
Haskett D, Johnson G, Zhou A, Utzinger U, Geest JV (2010) Microstructural and biomechanical alterations of the human aorta as a function of age and location. Biomech Model Mechanobiol 9: 725–736
Hayashi K, Handa H, Nagasawa S, Okumura A, Moritake K (1980) Stiffness and elastic behavior of human intracranial and extracranial arteries. J Biomech 13(2): 175–184
Hayenga HN (2010) Mechanics of atherosclerosis, hypertension-induced growth, and arterial remodeling. Ph.D. dissertation, Texas A&M University, TX, USA
Himwich WA, Spurgeon HA (1968) Pulse pressure contours in cerebral arteries. Acta Neurol Scand 44(1): 43–56
Hozumi T, Yoshida K, Akasaka T, Asami Y, Ogata Y, Takagi T, Kaji S, Kawamoto T, Ueda Y, Morioka S (1998) Noninvasive assessment of coronary flow velocity and coronary flow velocity reserve in the left anterior descending coronary artery by doppler echocardiography: comparison with invasive technique. J Am Coll Cardiol 32(5): 1251–1259
Hoffman MBM, Wickline SA, Lorenz CH (1998) Quantification of in-plane motion of the coronary arteries during the cardiac cycle: implications for acquisition window duration for MR flow quantification. JMRI 8(3): 568–576
Hu J-J, Ambrus A, Fossum TW, Miller MW, Humphrey JD, Wilson E (2008) Time courses of growth and remodeling of porcine aortic media during hypertension: a quantitative immunohistochemical examination. J Histochem Cytochem 56(4): 359–370
Hughes TJR (2000) The finite element method. Linear static and dynamic finite element analysis. Dover, New York
Huis GAV, Sipkema P, Westerhof N (1987) Coronary input impedance during cardiac cycle as determined by impulse response method. Am J Physiol 253(2 Pt 2): H317–H324
Humphrey JD (2002) Cardiovascular solid mechanics. Cells, tissues, and organs. Springer, New York
Humphrey JD (2008) Mechanisms of arterial remodeling in hypertension: coupled roles of wall shear and intramural stress. Hypertension 52(2): 195–200
Humphrey JD, Taylor CA (2008) Intracranial and abdominal aortic aneurysms: similarities, differences, and need for a new class of computational models. Annu Rev Biomed Eng 10: 221–246
Kim HJ, Figueroa CA, Hughes TJ, Jansen KE, Taylor CA (2009) Augmented lagrangian method for constraining the shape of velocity profiles at outlet boundaries for three-dimensional finite element simulations of blood flow. Comput Methods Appl Mech Eng 198: 3551–3566
Kim HJ, Vignon-Clementel IE, Coogan JS, Figueroa CA, Jansen KE, Taylor CA (2010) Patient-specific modeling of blood flow and pressure in human coronary arteries. Ann Biomed Eng 38(10): 3195–3209
Kim HJ, Vignon-Clementel IE, Figueroa CA, LaDisa JF, Jansen KE, Feinstein JA, Taylor CA (2009) On coupling a lumped parameter heart model and a three-dimensional finite element aorta model. Ann Biomed Eng 37(11): 2153–2169
LaDisa JF, Taylor CA, Feinstein JA (2010) Aortic coarctation: recent developments in experiemental and computational methods to assess treatments for this simple condition. Prog Pediatr Cardiol 30(1): 45–49
LaDisa JF, Figueroa CA, Vignon-Clementel IE, Kim HJ, Xiao N, Ellwein LM, Chan FP, Feinstein JA, Taylor CA (2011) Computational simulations for aortic coarctation: representative results from a sampling of patients. J Biomech Eng 133(9): 0910091
LaDisa JF, Dholakia RJ, Figueroa CA, Vignon-Clementel IE, Chan FP, Samyn MM, Cava JR, Taylor CA, Feinstein JA (2011) Computational simulations demonstrate altered wall shear stress in aortic coarctation patients previously treated by resection with end- to-end anastomosis. Congenit Heart Dis 6: 432–443
Lakatta EG, Wang M, Najjar SS (2009) Arterial aging and subclinical arterial disease are fundamentally intertwined at macroscopic and molecular levels. Med Clin N Am 93(3): 583–604 (Table of Contents)
Langille BL (1996) Arterial remodeling: relation to hemodynamics. Can J Physiol Pharmacol 74(7): 834–841
Lantz BM, Foerster JM, Link DP, Holcroft JW (1981) Regional distribution of cardiac output: normal values in man determined by video dilution technique. Am J Roentgenol 137(5): 903–907
Laurent S, Boutouyrie P, Lacolley P (2005) Structural and genetic bases of arterial stiffness. Hypertension 45(6): 1050–1055
Les AS, Shadden SC, Figueroa CA, Park JM, Tedesco MM, Herfkens RJ, Dalman RL, Taylor CA (2010) Quantification of hemodynamics in abdominal aortic aneurysms during rest and exercise using magnetic resonance imaging and computational fluid dynamics. Ann Biomed Eng 38(4): 1288–1313
Matsumoto T, Hayashi K (1994) Mechanical and dimensional adaptation of rat aorta to hypertension. J Biomech Eng 116(3): 278–283
Moghadam ME, Bazilevs Y, Hsia TY, Vignon-Clementel IE, Marsden AL (2011) A comparison of outlet boundary treatments for prevention of backflow divergence with relevance to blood flow simulations. Comput Mech 48(3): 277–291
Moireau P, Xiao N, Astorino M, Figueroa CA, Chapelle D, Taylor CA, Gerbeau J-F (2012) External tissue support and fluid-structure simulation in blood flows. Biomech Model Mechanobiol 11(1): 1–18
Nagai Y, Fleg JL, Kemper MK, Rywik TM, Earley CJ, Metter EJ (1999) Carotid arterial stiffness as a surrogate for aortic stiffness: relationship between carotid artery pressure-strain elastic modulus and aortic pulse wave velocity. Ultrasound Med Biol 25(2): 181–188
Nichols WW, O’Rourke MF (2005) McDonald’s blood flow in arteries: theoretical, experimental, and clinical principles. Hodder Arnold, London
O’Rourke MF, Hashimoto J (2007) Mechanical factors in arterial aging: a clinical perspective. J Am Coll Cardiol 50(1): 1–13
Osman NF, McVeigh ER, Prince JL (2000) Imaging heart motion using harmonic phase MRI. IEEE Trans Med Imag 19(3): 186–202
Ottesen J, Olufsen M, Larsen J (2004) Applied mathematical models in human physiology. SIAM, Philadelphia
Pearson GD, Devereux R, Loeys B, Maslen C, Milewicz D, Pyeritz R, Ramirez F, Rifkin D, Sakai L, Svensson L, Wessels A, Eyk JV, Dietz HC, National Heart L, Institute B, Group NMFW (2008) Report of the national heart, lung, and blood institute and national marfan foundation working group on research in marfan syndrome and related disorders. Circulation 118(7): 785–791
Prummer M, Fahrig R, Wigstrom L, Boese J, Lauritsch G, Strobel N, Hornegger J (2007) Cardiac C-arm CT: 4D non-model based heart motion estimation and its application. Proc SPIE 6510: 651015- 1-12
Redheuil A, Yu W-C, Wu CO, Mousseaux E, de Cesare A, Yan R, Kachenoura N, Bluemke D, Lima JAC (2010) Reduced ascending aortic strain and distensibility: earliest manifestations of vascular aging in humans. Hypertension 55(2): 319–326
Reymond P, Merenda F, Perren F, Rüfenacht D, Stergiopulos N (2009) Validation of a one-dimensional model of the systemic arterial tree. Am J Physiol Heart Circ Physiol 297(1): H208–H222
Safar ME (2000) Pulse pressure, arterial stiffness, and cardiovascular risk. Curr Opin Cardiol 15(4): 258–263
Safar ME (2010) Arterial aging–hemodynamic changes and therapeutic options. Nat Rev Cardiol 7(8): 442–449
Safar ME, Boudier HS (2005) Vascular development, pulse pressure, and the mechanisms of hypertension. Hypertension 46(1): 205–209
Sahni O, Muller J, Jansen KE, Shephard MS, Taylor CA (2006) Efficient anisotropic adaptive discretization of the cardiovascular system. Comput Methods Appl Mech Eng 195: 5634–5655
Scheel P, Ruge C, Petruch UR, Schöning M (2000) Color duplex measurement of cerebral blood flow volume in healthy adults. Stroke 31(1): 147–150
Schlosser T, Pagonidis K, Herborn CU, Hunold P, Waltering K-U, Lauenstein TC, Barkhausen J (2005) Assessment of left ventricular parameters using 16-mdct and new software for endocardial and epicardial border delineation. Am J Roentgenol 184(3): 765–773
Senzaki H, Chen CH, Kass DA (1996) Single-beat estimation of end-systolic pressure-volume relation in humans. a new method with the potential for noninvasive application. Circulation 94(10): 2497–2506
Simvascular: Cardiovascular Modeling and Simulation Application (2007) https://simtk.org/home/simvascular
Suga H, Sagawa K (1974) Instantaneous pressure–volume relationships and their ratio in the excised, supported canine left ventricle. Circ Res 35(1): 117–126
Suga H, Sagawa K, Shoukas AA (1973) Load independence of the instantaneous pressure–volume ratio of the canine left ventricle and effects of epinephrine and heart rate on the ratio. Circ Res 32(3): 314–322
Taylor CA, Figueroa CA (2009) Patient-specific modeling of cardiovascular mechanics. Annu Rev Biomed Eng 11: 109–134
Taylor SH, Donald KW (1960) Circulatory studies at rest and during exercise in coarctation of the aorta before and after operation. Br Heart J 22: 117–139
Toprea BI, Schwarzacher SP, Chang A, Asvar C, Huie P, Sibley RK, Zarins CK (2000) Reduction of aortic wall motion inhibits hypertension-mediated experimental atherosclerosis. Arterioscler Thromb Vasc Biol 20: 2127–2133
Valentín A, Baek S, Humphrey J (2009) Complementary roles of vasoactivity and matrix turnover in arterial adaptations to altered flow, pressure, and axial stretch. J R Soc Interface 6: 293–306
Vignon-Clementel IE, Figueroa CA, Jansen KE, Taylor CA (2006) Outflow boundary conditions for three-dimensional finite element modeling of blood flow and pressure in arteries. Comput Methods Appl Mech Eng 195: 3776–3796
Wagner HP, Humphrey JD (2011) Differential passive and active biaxial mechanical behaviors of muscular and elastic arteries: basilar versus common carotid. J Biomech Eng 133(5): 051009
Weissler AM, Harris LC, White GD (1963) Left ventricular ejection time index in man. J Appl Physiol 18: 919–923
Whiting C, Jansen K (2001) A stabilized finite element method for the incompressible navier-stokes equations using a hierarchical basis. Int J Numer Methods Flds 35: 93–116
Williams LR, Leggett RW (1989) Referece values for resting blood flow to organs of man. Clin Phys Physiol Meas 10(3): 187–217
Wilson N, Wang K, Dutton RW, Taylor CA (2001) A software framework for creating patient specific geometric models from medical imaging data for simulation based medical planning of vascular surgery. Lect Notes Comput Sci 2208: 449–456
Wolinsky H (1970) Response of the rat aortic media to hypertension. morphological and chemical studies. Circ Res 26(4): 507–522
Wolinsky H (1972) Long-term effects of hypertension on the rat aortic wall and their relation to concurrent aging changes. Morphological and chemical studies. Circ Res 30(3): 301–309
Xiong G, Figueroa CA, Xiao N, Taylor CA (2011) Simulation of blood flow in deformable vessels using subject-specific geometry and assigned variable mechanical wall properties. Int J Numer Methods Biomed Eng 27: 1000–1016
Xu C, Zarins CK, Bassiouny HS, Briggs WH, Reardon C, Glagov S (2000) Differential transmural distribution of gene expression for collagen types i and iii proximal to aortic coarctation in the rabbit. J Vasc Res 37(3): 170–182
Zamir M, Sinclair P, Wonnacott TH (1992) Relation between diameter and flow in major branches of the arch of the aorta. J Biomech 25(11): 1303–1310
Zhang DP, Edwards E, Mei L, Rueckert D (2009) 4D Motion modeling of the coronary arteries from CT images for robotic assited minimally invasive surgery. Proc SPIE 7259: 72590X-1-8
Zhou Y, Kassab GS, Molloi S (1999) On the design of the coronary arterial tree: a generalization of Murray’s law. Phys Med Biol 44(12): 2929–2945
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Coogan, J.S., Humphrey, J.D. & Figueroa, C.A. Computational simulations of hemodynamic changes within thoracic, coronary, and cerebral arteries following early wall remodeling in response to distal aortic coarctation. Biomech Model Mechanobiol 12, 79–93 (2013). https://doi.org/10.1007/s10237-012-0383-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10237-012-0383-x