Skip to main content
Log in

A multiphysics approach for modeling early atherosclerosis

  • Original Paper
  • Published:
Biomechanics and Modeling in Mechanobiology Aims and scope Submit manuscript

Abstract

This work is devoted to the development of a mathematical model of the early stages of atherosclerosis incorporating processes of all time scales of the disease and to show their interactions. The cardiovascular mechanics is modeled by a fluid–structure interaction approach coupling a non-Newtonian fluid to a hyperelastic solid undergoing anisotropic growth and a change of its constitutive equation. Additionally, the transport of low-density lipoproteins and its penetration through the endothelium is considered by a coupled set of advection–diffusion-reaction equations. Thereby, the permeability of the endothelium is wall-shear stress modulated resulting in a locally varying accumulation of foam cells triggering a novel growth and remodeling formulation. The model is calibrated and applied to an murine-specific case study, and a qualitative validation of the computational results is performed. The model is utilized to further investigate the influence of the pulsatile blood flow and the compliance of the artery wall to the atherosclerotic process. The computational results imply that the pulsatile blood flow is crucial, whereas the compliance of the aorta has only a minor influence on atherosclerosis. Further, it is shown that the novel model is capable to produce a narrowing of the vessel lumen inducing an adaption of the endothelial permeability pattern.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14

Similar content being viewed by others

Notes

  1. Wall-shear stresses is the established name even though wall-shear tractions would be more accurate

References

  • Ambrosi D, Mollica F (2002) On the mechanics of a growing tumor. Int J Eng Sci 40(12):1297–1316

    Article  MathSciNet  MATH  Google Scholar 

  • Arora D (2005) Computational hemodynamics: Hemolysis and viscoelasticity. Ph.D. thesis, Citeseer

  • Asakura T, Karino T (1990) Flow patterns and spatial distribution of atherosclerotic lesions in human coronary arteries. Circ Res 66(4):1045–1066

    Article  Google Scholar 

  • Aslanidou L, Trachet B, Reymond P, Fraga-Silva RA, Segers P, Stergiopulos N (2016) A 1D model of the arterial circulation in mice. ALTEX 33(1):13

    Article  Google Scholar 

  • Balzani D, Schmidt T (2015) Comparative analysis of damage functions for soft tissues: properties at damage initialization. Math Mech Solids 20(4):480–492

    Article  MathSciNet  MATH  Google Scholar 

  • Barrenechea GR, Valentin F (2002) An unusual stabilized finite element method for a generalized stokes problem. Numer Math 92(4):653–677

    Article  MathSciNet  MATH  Google Scholar 

  • Bazilevs Y, Calo VM, Tezduyar TE, Hughes TJ (2007) YZ\(\beta \) discontinuity capturing for advection-dominated processes with application to arterial drug delivery. Int J Numer Methods Fluids 54:593–608

    Article  MathSciNet  MATH  Google Scholar 

  • Bazilevs Y, Gohean J, Hughes T, Moser R, 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):3534–3550

    Article  MathSciNet  MATH  Google Scholar 

  • Bird RB, Armstrong R, Hassager O (1987) Dynamics of polymeric liquids, vol 1. Fluid mechanics. Wiley, New York

    Google Scholar 

  • Brown AJ, Teng Z, Evans PC, Gillard JH, Samady H, Bennett MR (2016) Role of biomechanical forces in the natural history of coronary atherosclerosis. Nat Rev Cardiol 13:210–220

    Article  Google Scholar 

  • Calvez V, Houot JG, Meunier N, Raoult A, Rusnakova G (2010) Mathematical and numerical modeling of early atherosclerotic lesions. ESAIM Proc Surv 30:14. https://doi.org/10.1051/proc/2010002

    Article  MathSciNet  MATH  Google Scholar 

  • Carew TE, VAISHNAV RN, PATEL DJ (1968) Compressibility of the arterial wall. Circ Res 23(1):61–68

    Article  Google Scholar 

  • Chalmers AD, Cohen A, Bursill CA, Myerscough MR (2015) Bifurcation and dynamics in a mathematical model of early atherosclerosis. J Math Biol 71(6–7):1451–1480

    Article  MathSciNet  MATH  Google Scholar 

  • Chen J, Lu XY (2006) Numerical investigation of the non-newtonian pulsatile blood flow in a bifurcation model with a non-planar branch. J Biomech 39(5):818–832

    Article  Google Scholar 

  • Cheng C, Helderman F, Tempel D, Segers D, Hierck B, Poelmann R, van Tol A, Duncker DJ, Robbers-Visser D, Ursem NT et al (2007) Large variations in absolute wall shear stress levels within one species and between species. Atherosclerosis 195(2):225–235

    Article  Google Scholar 

  • Cho YI, Kensey KR (1991) Effects of the non-newtonian viscosity of blood on flows in a diseased arterial vessel. Part 1: steady flows. Biorheology 28:241–62

    Article  Google Scholar 

  • Cilla M, Peña E, Martínez MA (2014) Mathematical modelling of atheroma plaque formation and development in coronary arteries. J R Soc Interface 11(90):20130,866

    Article  Google Scholar 

  • Codina R (2002) Stabilized finite element approximation of transient incompressible flows using orthogonal subscales. Comput Methods Appl Mech Eng 191(39):4295–4321

    Article  MathSciNet  MATH  Google Scholar 

  • Crosetto P, Reymond P, Deparis S, Kontaxakis D, Stergiopulos N, Quarteroni A (2011) Fluid–structure interaction simulation of aortic blood flow. Comput Fluids 43(1):46–57

    Article  MathSciNet  MATH  Google Scholar 

  • De Souza Neto E, Perić D, Dutko M, Owen D (1996) Design of simple low order finite elements for large strain analysis of nearly incompressible solids. Int J Solids Struct 33(20):3277–3296

    MathSciNet  MATH  Google Scholar 

  • De Wilde D, Trachet B, De Meyer GR, Segers P (2015a) Shear stress metrics and their relation to atherosclerosis: an in vivo follow-up study in atherosclerotic mice. Ann Biomed Eng 44:2327–2388

    Article  Google Scholar 

  • De Wilde D, Trachet B, Debusschere N, Iannaccone F, Swillens A, Degroote J, Vierendeels J, De Meyer GR, Segers P (2015b) Assessment of shear stress related parameters in the carotid bifurcation using mouse-specific FSI simulations. J Biomech 49:2135–2142

    Article  Google Scholar 

  • De Wilde D, Trachet B, De Meyer G, Segers P (2016) The influence of anesthesia and fluid–structure interaction on simulated shear stress patterns in the carotid bifurcation of mice. J Biomech 49(13):2741–2747

    Article  Google Scholar 

  • Dobrin PB, Rovick AA (1969) Influence of vascular smooth muscle on contractile mechanics and elasticity of arteries. Am J Physiol Leg Content 217(6):1644–1651

    Article  Google Scholar 

  • Doll S, Schweizerhof K (2000) On the development of volumetric strain energy functions. J Appl Mech 67(1):17–21

    Article  MATH  Google Scholar 

  • Doll S, Schweizerhof K, Hauptmann R, Freischläger C (2000) On volumetric locking of low-order solid and solid-shell elements for finite elastoviscoplastic deformations and selective reduced integration. Eng Comput 17(7):874–902

    Article  MATH  Google Scholar 

  • Donea J, Huerta A (2003) Finite element methods for flow problems. Wiley, Hoboken

    Book  Google Scholar 

  • Donea J, Giuliani S, Halleux J (1982) An arbitrary lagrangian-eulerian finite element method for transient dynamic fluid–structure interactions. Comput Methods Appl Mech Eng 33(1):689–723

    Article  MATH  Google Scholar 

  • Faxon DP, Fuster V, Libby P, Beckman JA, Hiatt WR, Thompson RW, Topper JN, Annex BH, Rundback JH, Fabunmi RP et al (2004) Atherosclerotic vascular disease conference writing group iii: pathophysiology. Circulation 109(21):2617–2625

    Article  Google Scholar 

  • Feintuch A, Ruengsakulrach P, Lin A, Zhang J, Zhou YQ, Bishop J, Davidson L, Courtman D, Foster FS, Steinman DA et al (2007) Hemodynamics in the mouse aortic arch as assessed by MRI, ultrasound, and numerical modeling. Am J Physiol Heart Circ Physiol 292(2):H884–H892

    Article  Google Scholar 

  • Ferruzzi J, Bersi M, Humphrey J (2013) Biomechanical phenotyping of central arteries in health and disease: advantages of and methods for murine models. Ann Biomed Eng 41(7):1311–1330

    Article  Google Scholar 

  • Figueroa CA, Baek S, Taylor CA, Humphrey JD (2009) A computational framework for fluid–solid-growth modeling in cardiovascular simulations. Comput Methods Appl Mech Eng 198(45–46):3583–3602. https://doi.org/10.1016/j.cma.2008.09.013

    Article  MathSciNet  MATH  Google Scholar 

  • Filipovic N, Rosic M, Tanaskovic I, Parodi O, Fotiadis D (2011) Computer simulation and experimental analysis of LDL transport in the arteries. In: Engineering in medicine and biology society, EMBC, 2011 Annual International Conference of the IEEE. IEEE, pp 195–198

  • Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18(6):499–502

    Google Scholar 

  • Friedman A, Hao W (2015) A mathematical model of atherosclerosis with reverse cholesterol transport and associated risk factors. Bull Math Biol 77(5):758–781

    Article  MathSciNet  MATH  Google Scholar 

  • Gee M, Förster C, Wall W (2010) A computational strategy for prestressing patient-specific biomechanical problems under finite deformation. Int J Numer Methods Biomed Eng 26(1):52–72

    Article  MATH  Google Scholar 

  • Gee MW, Küttler U, Wall WA (2011) Truly monolithic algebraic multigrid for fluid–structure interaction. Int J Numer Methods Eng 85(8):987–1016

    Article  MathSciNet  MATH  Google Scholar 

  • Gijsen F, Allanic E, Van de Vosse F, Janssen J (1999) The influence of the non-newtonian properties of blood on the flow in large arteries: unsteady flow in a 90 curved tube. J Biomech 32(7):705–713

    Article  Google Scholar 

  • Goriely A, Amar MB (2007) On the definition and modeling of incremental, cumulative, and continuous growth laws in morphoelasticity. Biomech Model Mechanobiol 6(5):289–296

    Article  Google Scholar 

  • Gravemeier V, Comerford A, Yoshihara L, Ismail M, Wall WA (2012) A novel formulation for Neumann inflow boundary conditions in biomechanics. Int J Numer Methods Biomed Eng 28(5):560–573

    Article  MathSciNet  MATH  Google Scholar 

  • 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(6):725–736

    Article  Google Scholar 

  • Heiland VM, Forsell C, Roy J, Hedin U, Gasser TC (2013) Identification of carotid plaque tissue properties using an experimental-numerical approach. J Mech Behav Biomed Mater 27:226–238

    Article  Google Scholar 

  • Herrmann RA, Malinauskas RA, Truskey GA (1994) Characterization of sites with elevated ldl permeability at intercostal, celiac, and iliac branches of the normal rabbit aorta. Arterioscler Thromb Vasc Biol 14(2):313–323

    Article  Google Scholar 

  • Himburg HA, Grzybowski DM, Hazel AL, LaMack JA, Li XM, Friedman MH (2004) Spatial comparison between wall shear stress measures and porcine arterial endothelial permeability. Am J Physiol Heart Circ Physiol 286(5):H1916–H1922

    Article  Google Scholar 

  • Holzapfel GA, Gasser TC, Ogden RW (2000) A new constitutive framework for arterial wall mechanics and a comparative study of material models. J Elast Phys Sci Solids 61(1–3):1–48

    MathSciNet  MATH  Google Scholar 

  • Holzapfel GA, Mulvihill JJ, Cunnane EM, Walsh MT (2014) Computational approaches for analyzing the mechanics of atherosclerotic plaques: a review. J Biomech 47(4):859–869

    Article  Google Scholar 

  • Hossain SS, Hossainy SF, Bazilevs Y, Calo VM, Hughes TJ (2012) Mathematical modeling of coupled drug and drug-encapsulated nanoparticle transport in patient-specific coronary artery walls. Comput Mech 49(2):213–242

    Article  MathSciNet  MATH  Google Scholar 

  • Humphrey J (2002) Cardiovascular solid mechanics: cells, tissues, and organs. Springer, Berlin

    Book  Google Scholar 

  • Huo Y, Guo X, Kassab GS (2008) The flow field along the entire length of mouse aorta and primary branches. Ann Biomed Eng 36(5):685–699

    Article  Google Scholar 

  • Ismail M, Wall WA, Gee MW (2013) Adjoint-based inverse analysis of windkessel parameters for patient-specific vascular models. J Comput Phys 244:113–130

    Article  MathSciNet  MATH  Google Scholar 

  • Ismail M, Gravemeier V, Comerford A, Wall W (2014) A stable approach for coupling multidimensional cardiovascular and pulmonary networks based on a novel pressure-flow rate or pressure-only Neumann boundary condition formulation. Int J Numer Methods Biomed Eng 30(4):447–469

    Article  MathSciNet  Google Scholar 

  • Johnston BM, Johnston PR, Corney S, Kilpatrick D (2004) Non-Newtonian blood flow in human right coronary arteries: steady state simulations. J Biomech 37(5):709–720

    Article  Google Scholar 

  • Južnič G, Klensch H (1964) Vergleichend-physiologische Untersuchungen über das Verhalten der Indices für Energieaufwand und Leistung des Herzens. Pflüger’s Archiv für die gesamte Physiologie des Menschen und der Tiere 280(1):38–45

    Article  Google Scholar 

  • Karimi R, Zhu T, Bouma BE, Mofrad MRK (2008) Estimation of nonlinear mechanical properties of vascular tissues via elastography. Cardiovasc Eng 8(4):191–202

    Article  Google Scholar 

  • Karner G, Perktold K (2000) Effect of endothelial injury and increased blood pressure on albumin accumulation in the arterial wall: a numerical study. J Biomech 33(6):709–715

    Article  Google Scholar 

  • Kedem O, Katchalsky A (1958) Thermodynamic analysis of the permeability of biological membranes to non-electrolytes. Biochim Biophys Acta 27:229–246

    Article  Google Scholar 

  • Klisch SM, Van Dyke TJ, Hoger A (2001) A theory of volumetric growth for compressible elastic biological materials. Math Mech Solids 6(6):551–575

    Article  MATH  Google Scholar 

  • Klöppel T, Popp A, Küttler U, Wall WA (2011) Fluid–structure interaction for non-conforming interfaces based on a dual mortar formulation. Comput Methods Appl Mech Eng 200(45):3111–3126

    Article  MathSciNet  MATH  Google Scholar 

  • Koshiba N, Ando J, Chen X, Hisada T (2007) Multiphysics simulation of blood flow and LDL transport in a porohyperelastic arterial wall model. J Biomech Eng 129(3):374–385

    Google Scholar 

  • Ku DN, Giddens DP, Zarins CK, Glagov S (1985) Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arterioscler Thromb Vasc Biol 5(3):293–302

    Article  Google Scholar 

  • Kuhl E, Maas R, Himpel G, Menzel A (2007) Computational modeling of arterial wall growth. Biomech Model Mechanobiol 6(5):321–331

    Article  Google Scholar 

  • Küttler U, Gee M, Förster C, Comerford A, Wall W (2010) Coupling strategies for biomedical fluid–structure interaction problems. Int J Numer Methods Biomed Eng 26(3–4):305–321

    Article  MathSciNet  MATH  Google Scholar 

  • Kuzmin D (2010) A guide to numerical methods for transport equations. University Erlangen-Nuremberg, Erlangen

    Google Scholar 

  • Lee SW, Antiga L, Spence JD, Steinman DA (2008) Geometry of the carotid bifurcation predicts its exposure to disturbed flow. Stroke 39(8):2341–2347

    Article  Google Scholar 

  • Liu M, Tang H, Nicholson JK, Lindon JC (2002) Use of 1H NMR-determined diffusion coefficients to characterize lipoprotein fractions in human blood plasma. Magn Reson Chem 40(13):S83–S88

    Article  Google Scholar 

  • Liu Y, Dang C, Garcia M, Gregersen H, Kassab GS (2007) Surrounding tissues affect the passive mechanics of the vessel wall: theory and experiment. Am J Physiol Heart Circ Physiol 293(6):H3290–H3300

    Article  Google Scholar 

  • Liu X, Fan Y, Deng X (2010) Effect of spiral flow on the transport of oxygen in the aorta: a numerical study. Ann Biomed Eng 38(3):917–926

    Article  Google Scholar 

  • Liu X, Fan Y, Deng X, Zhan F (2011) Effect of non-Newtonian and pulsatile blood flow on mass transport in the human aorta. J Biomech 44(6):1123–1131

    Article  Google Scholar 

  • Loree HM, Tobias BJ, Gibson LJ, Kamm RD, Small DM, Lee RT (1994) Mechanical properties of model atherosclerotic lesion lipid pools. Arterioscler Thromb Vasc Biol 14(2):230–234

    Article  Google Scholar 

  • Lutgens E, Lievens D, Beckers L, Wijnands E, Soehnlein O, Zernecke A, Seijkens T, Engel D, Cleutjens J, Keller AM et al (2010) Deficient CD40-TRAF6 signaling in leukocytes prevents atherosclerosis by skewing the immune response toward an antiinflammatory profile. J Exp Med 207(2):391–404

    Article  Google Scholar 

  • Mayr M, Klöppel T, Wall WA, Gee MW (2015) A temporal consistent monolithic approach to fluid-structure interaction enabling single field predictors. SIAM J Sci Comput 37(1):B30–B59

    Article  MathSciNet  MATH  Google Scholar 

  • Moireau P, Xiao N, Astorino M, Figueroa CA, Chapelle D, Taylor CA, Gerbeau JF (2012) External tissue support and fluid–structure simulation in blood flows. Biomech Model Mechanobiol 11(1–2):1–18

    Article  Google Scholar 

  • Nadkarni SK, Bouma BE, Helg T, Chan R, Halpern E, Chau A, Minsky MS, Motz JT, Houser SL, Tearney GJ (2005) Characterization of atherosclerotic plaques by laser speckle imaging. Circulation 112(6):885–892

    Article  Google Scholar 

  • Ogden R (1972) Large deformation isotropic elasticity-on the correlation of theory and experiment for incompressible rubberlike solids. In: Proceedings of the royal society of London A: mathematical, physical and engineering sciences, The Royal Society, vol. 326, pp 565–584

  • Ogden R (1978) Nearly isochoric elastic deformations: application to rubberlike solids. J Mech Phys Solids 26(1):37–57

    Article  MathSciNet  MATH  Google Scholar 

  • Olgac U, Poulikakos D, Saur SC, Alkadhi H, Kurtcuoglu V (2009) Patient-specific three-dimensional simulation of LDL accumulation in a human left coronary artery in its healthy and atherosclerotic states. Am J Physiol Heart Circ Physiol 296(6):H1969–H1982

    Article  Google Scholar 

  • Olshanskii M, Lube G, Heister T, Löwe J (2009) Grad-div stabilization and subgrid pressure models for the incompressible Navier–Stokes equations. Comput Methods Appl Mech Eng 198(49):3975–3988

    Article  MathSciNet  MATH  Google Scholar 

  • Olufsen MS, Peskin CS, Kim WY, Pedersen EM, Nadim A, Larsen J (2000) Numerical simulation and experimental validation of blood flow in arteries with structured-tree outflow conditions. Ann Biomed Eng 28(11):1281–1299

    Article  Google Scholar 

  • Ougrinovskaia A, Thompson RS, Myerscough MR (2010) An ode model of early stages of atherosclerosis: mechanisms of the inflammatory response. Bull Math Biol 72(6):1534–61. https://doi.org/10.1007/s11538-010-9509-4

    Article  MathSciNet  MATH  Google Scholar 

  • Parton A, McGilligan V, O’Kane M, Baldrick FR, Watterson S (2016) Computational modelling of atherosclerosis. Brief Bioinform 17(4): 562–575. https://doi.org/10.1093/bib/bbv081

  • Peiffer V, Sherwin SJ, Weinberg PD (2013) Does low and oscillatory wall shear stress correlate spatially with early atherosclerosis? a systematic review. Cardiovasc Res 99(2):242–250. https://doi.org/10.1093/cvr/cvt044

  • Prosi M, Zunino P, Perktold K, Quarteroni A (2005) Mathematical and numerical models for transfer of low-density lipoproteins through the arterial walls: a new methodology for the model set up with applications to the study of disturbed lumenal flow. J Biomech 38(4):903–917

    Article  Google Scholar 

  • Resnick N, Yahav H, Shay-Salit A, Shushy M, Schubert S, Zilberman LCM, Wofovitz E (2003) Fluid shear stress and the vascular endothelium: for better and for worse. Prog Biophys Mol Biol 81(3):177–199

    Article  Google Scholar 

  • Roccabianca S, Figueroa C, Tellides G, Humphrey J (2014) Quantification of regional differences in aortic stiffness in the aging human. J Mech Behav Biomed Mater 29:618–634

    Article  Google Scholar 

  • Ross R (1999) Atherosclerosis—an inflammatory disease. N Engl J Med 340(2):115–126

    Article  Google Scholar 

  • Saad Y, Schultz MH (1986) GMRES: a generalized minimal residual algorithm for solving nonsymmetric linear systems. SIAM J Sci Stat Comput 7(3):856–869

    Article  MathSciNet  MATH  Google Scholar 

  • Sansour C (2008) On the physical assumptions underlying the volumetric-isochoric split and the case of anisotropy. Eur J Mech A Solids 27(1):28–39

    Article  MathSciNet  MATH  Google Scholar 

  • Skalak R, Zargaryan S, Jain RK, Netti PA, Hoger A (1996) Compatibility and the genesis of residual stress by volumetric growth. J Math Biol 34(8):889–914

    Article  MATH  Google Scholar 

  • Smith N, Pullan A, Hunter PJ (2002) An anatomically based model of transient coronary blood flow in the heart. SIAM J Appl Math 62(3):990–1018

    Article  MathSciNet  MATH  Google Scholar 

  • Soulis JV, Lampri OP, Fytanidis DK, Giannoglou GD (2011) Relative residence time and oscillatory shear index of non-Newtonian flow models in aorta. In: 2011 10th international workshop on biomedical engineering, IEEE, pp 1–4

  • Stangeby DK, Ethier CR (2002) Computational analysis of coupled blood-wall arterial LDL transport. J Biomech Eng 124(1):1–8

    Article  Google Scholar 

  • Stocker R, Keaney JF (2004) Role of oxidative modifications in atherosclerosis. Physiol Rev 84(4):1381–1478

    Article  Google Scholar 

  • Sun N, Wood NB, Hughes AD, Thom SAM, Xu XY (2007) Influence of pulsatile flow on ldl transport in the arterial wall. Ann Biomed Eng 35(10):1782–90. https://doi.org/10.1007/s10439-007-9347-1

    Article  Google Scholar 

  • Suo J, Ferrara DE, Sorescu D, Guldberg RE, Taylor WR, Giddens DP (2007) Hemodynamic shear stresses in mouse aortas implications for atherogenesis. Arterioscler Thromb Vasc Biol 27(2):346–351

    Article  Google Scholar 

  • Thomas SR, Mikulecky DC (1978) Transcapillary solute exchange: a comparison of the kedem-katchalsky convection–diffusion equations with the rigorous nonlinear equations for this special case. Microvasc Res 15(2):207–220

    Article  Google Scholar 

  • Tomaso GD, Díaz-Zuccarini V, Pichardo-Almarza C (2011) A multiscale model of atherosclerotic plaque formation at its early stage. IEEE Trans Biomed Eng 58(12):3460–3463

    Article  Google Scholar 

  • Tompkins RG (1991) Quantitative analysis of blood vessel permeability of squirrel monkeys. Am J Physiol Heart Circ Physiol 260(4):H1194–H1204

    Article  Google Scholar 

  • Truskey GA, Roberts WL, Herrmann RA, Malinauskas RA (1992) Measurement of endothelial permeability to 125i-low density lipoproteins in rabbit arteries by use of en face preparations. Circ Res 71(4):883–897

    Article  Google Scholar 

  • Wada S, Koujiya M, Karino T (2002) Theoretical study of the effect of local flow disturbances on the concentration of low-density lipoproteins at the luminal surface of end-to-end anastomosed vessels. Med Biol Eng Compu 40(5):576–587

    Article  Google Scholar 

  • Wall W, Gee M (2010) Baci: a parallel multiphysics finite element environment. Technische Universität München, Institute for Computational Mechanics

  • Wang W, Lee Y, Lee CH (2013) Review: the physiological and computational approaches for atherosclerosis treatment. Int J Cardiol 167(5):1664–1676

    Article  Google Scholar 

  • Westerhof N, Lankhaar JW, Westerhof BE (2009) The arterial windkessel. Med Biol Eng Comput 47(2):131–141

    Article  Google Scholar 

  • Whitesall SE, Hoff JB, Vollmer AP, D’Alecy LG (2004) Comparison of simultaneous measurement of mouse systolic arterial blood pressure by radiotelemetry and tail-cuff methods. Am J Physiol Heart Circ Physiol 286(6):H2408–H2415

    Article  Google Scholar 

  • Wiesmann F, Szimtenings M, Frydrychowicz A, Illinger R, Hunecke A, Rommel E, Neubauer S, Haase A (2003) High-resolution mri with cardiac and respiratory gating allows for accurate in vivo atherosclerotic plaque visualization in the murine aortic arch. Magn Reson Med 50(1):69–74

    Article  Google Scholar 

  • Xiao N, Alastruey J, Alberto Figueroa C (2014) A systematic comparison between 1-D and 3-D hemodynamics in compliant arterial models. Int J Numer Methods Biomed Eng 30(2):204–31. https://doi.org/10.1002/cnm.2598

    Article  MathSciNet  Google Scholar 

  • Yang N, Vafai K (2006) Modeling of low-density lipoprotein (LDL) transport in the artery—effects of hypertension. Int J Heat Mass Transf 49(5):850–867

    Article  MATH  Google Scholar 

  • Yang Y, Richter T, Jäger W, Neuss-Radu M (2016) An ALE approach to mechano-chemical processes in fluid-structure interactions. Int J Numer Methods Fluids 84:199–220

  • Yoshihara L, Coroneo M, Comerford A, Bauer G, Klöppel T, Wall W (2014) A combined fluid–structure interaction and multi-field scalar transport model for simulating mass transport in biomechanics. Int J Numer Methods Eng 100(4):277–299

    Article  MathSciNet  MATH  Google Scholar 

  • Zareh M, Fradet G, Naser G, Mohammadi H (2015) Are two-dimensional images sufficient to assess the atherosclerotic plaque vulnerability: a viscoelastic and anisotropic finite element model. Cardiovasc Syst 3(1):3

    Article  Google Scholar 

  • Zunino P (2002) Mathematical and numerical modeling of mass transfer in the vascular system. Ph.D. thesis, Politecnico di Milano

Download references

Acknowledgements

The authors gratefully acknowledge the financial support given by the International Graduate School of Science and Engineering of the Technical University of Munich under the project BioMat01, A Multiscale Model of Atherosclerosis. This work was supported by the German Research Foundation (DFG) and the Technical University of Munich (TUM) in the framework of the Open Access Publishing Program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. W. Gee.

Ethics declarations

Conflict of interest

All authors declare that no conflicts of interest exist.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thon, M.P., Hemmler, A., Glinzer, A. et al. A multiphysics approach for modeling early atherosclerosis. Biomech Model Mechanobiol 17, 617–644 (2018). https://doi.org/10.1007/s10237-017-0982-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-017-0982-7

Keywords

Navigation