Skip to main content
SpringerLink
Log in

Contribution of atherosclerotic plaque location and severity to the near-wall hemodynamics of the carotid bifurcation: an experimental study and FSI modeling

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

Abstract

Atherosclerosis is initiated by endothelial injury that is related to abnormal values of hemodynamic parameters such as wall shear stress (WSS), oscillatory shear index (OSI) and stress phase angle (SPA), which are more common in arterial bifurcations due to the complex structure. An experimental model of human carotid bifurcation with accurate geometrical and mechanical features was set up, and using realistic pulsatile flow rates, the inlet and outlet pressure pulses were measured for normal and stenosed models with 40% and 80% severities at common carotid (CCA), internal carotid (ICA) and external carotid (ECA) arteries. Based on the obtained experimental data, fluid–structure models were developed to obtain WSS, OSI, and SPA and evaluate pathological consequences at different locations. Mild severity had minor impact, however, inducing severe 80% stenosis in each branch led to considerable localized changes of hemodynamic parameters both in the stenosis site and other locations. This included sharp increases in WSS values accompanied by very low values close to zero before and after the peaks. Severe stenosis not only caused significant changes in the local artery, but also in other branches. OSI and SPA were less sensitive to stenosis, although high peaks were observed on bifurcation site for the stenosis at ECA. The interconnection of arteries at carotid bifurcation results in altered pressure/flow patterns in all branches when a stenosis is applied in any site. Such effect confirms pathological findings that atherosclerotic plaques are observed simultaneously in different carotid branches, although with different degrees of plaque growth and severity.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Amaya R, Pierides A, Tarbell JM (2015) The interaction between fluid wall shear stress and solid circumferential strain affects endothelial gene expression. PloS One 10(7):e0129952

    Google Scholar 

  • Amaya R, Cancel LM, Tarbell JM (2016) Interaction between the stress phase angle (SPA) and the oscillatory shear index (OSI) affects endothelial cell gene expression. PloS One 11(11):e0166569

    Google Scholar 

  • Amini S, Tafazzoli-Shadpour M, Haghighipour N, Golpayegani MRH , Shokrgozar MA (2008) Study of Tensile Cyclic Loading on Morphology of Endothelial Cell Line in Culture Medium: A Fractal and Topological Comparison. CMBES Proceedings, p. 31.

  • Arzani A, Shadden SC (2018) Wall shear stress fixed points in cardiovascular fluid mechanics. J Biomech 73:145–152

    Google Scholar 

  • Assemat P, Armitage JA, Siu KK, Contreras KG, Dart AM, Chin-Dusting JP, Hourigan K (2014) Three-dimensional numerical simulation of blood flow in mouse aortic arch around atherosclerotic plaques. Appl Math Model 38(17–18):4175–4185

    MathSciNet  Google Scholar 

  • Atabek HB, Ling SC, Patel DJ (1975) Analysis of coronary flow fields in thoracotomized dogs. Circ Res 37(6):752–761

    Google Scholar 

  • Ballermann BJ, Dardik A, Eng E, Liu A (1998) Shear stress and the endothelium. Kidney Int Suppl 67:S100-108

    Google Scholar 

  • Berne RM, Winn HR, Rubio R (1981) The local regulation of cerebral blood flow. Prog Cardiovasc Dis 24(3):243–260

    Google Scholar 

  • Birchall D, Zaman A, Hacker J, Davies G, Mendelow D (2006) Analysis of haemodynamic disturbance in the atherosclerotic carotid artery using computational fluid dynamics. Eur Radiol 16(5):1074–1083

    Google Scholar 

  • Charkoudian N (2010) Mechanisms and modifiers of reflex induced cutaneous vasodilation and vasoconstriction in humans. J Appl Physiol 109(4):1221–1228

    Google Scholar 

  • Chistiakov DA, Orekhov AN, Bobryshev YV (2017) Effects of shear stress on endothelial cells: go with the flow. Acta Physiol 219(2):382–408

    Google Scholar 

  • Clemente G, Mancini M, Giacco R, Tornatore A, Ragucci M, Riccardi G (2015) Visceral adiposity and subclinical atherosclerosis in healthy young men. Int J Food Sci Nutr 66(4):466–470

    Google Scholar 

  • Dancu MB, Tarbell JM (2006) Large negative stress phase angle (SPA) attenuates nitric oxide production in bovine aortic endothelial cells. J Biomech Eng 128(3):329–334

    Google Scholar 

  • De Nisco G, Hoogendoorn A, Chiastra C, Gallo D, Kok AM, Morbiducci U, Wentzel JJ (2020a) The impact of helical flow on coronary atherosclerotic plaque development. Atherosclerosis 300:39–46

    Google Scholar 

  • De Nisco G, Tasso P, Calo K, Mazzi V, Gallo D, Condemi F, Farzaneh S, Avril S, Morbiducci U (2020b) Deciphering ascending thoracic aortic aneurysm hemodynamics in relation to biomechanical properties. Med Eng Phys 82:119–129

    Google Scholar 

  • Dejana E, Hirschi KK, Simons M (2017) The molecular basis of endothelial cell plasticity. Nat Commun 8(1):14361

    Google Scholar 

  • DiCarlo AL, Holdsworth DW, Poepping TL (2019) Study of the effect of stenosis severity and non-Newtonian viscosity on multidirectional wall shear stress and flow disturbances in the carotid artery using particle image velocimetry. Med Eng Phys 65:8–23

    Google Scholar 

  • Domanin M, Gallo D, Vergara C, Biondetti P, Forzenigo LV, Morbiducci U (2019) Prediction of long term restenosis risk after surgery in the carotid bifurcation by hemodynamic and geometric analysis. Ann Biomed Eng 47(4):1129–1140

    Google Scholar 

  • Donea J, Huerta A, Ponthot JP, Rodríguez-Ferran A (2017) Arbitrary L agrangian–E ulerian Methods. Encycl Comput Mech Second Edn. https://doi.org/10.1002/9781119176817.ecm2009

    Article  Google Scholar 

  • Eikendal AL, Groenewegen KA, Bots ML, Peters SA, Uiterwaal CS, den Ruijter HM (2016) Relation between adolescent cardiovascular risk factors and carotid intima-media echogenicity in healthy young adults: the atherosclerosis risk in young adults (ARYA) study. J Am Heart Assoc 5(5):e002941

    Google Scholar 

  • Gallo D, Steinman DA, Morbiducci U (2016) Insights into the co-localization of magnitude-based versus direction-based indicators of disturbed shear at the carotid bifurcation. J Biomech 49(12):2413–2419

    Google Scholar 

  • Gallo D, Bijari PB, Morbiducci U, Qiao Y, Xie Y, Etesami M, Habets D, Lakatta EG, Wasserman BA, Steinman DA (2018) Segment-specific associations between local haemodynamic and imaging markers of early atherosclerosis at the carotid artery: an in vivo human study. J R Soc Interface 15(147):20180352

    Google Scholar 

  • Giacomin AJ, Dealy JM (1993) Large-amplitude oscillatory shear. In: Collyer AA (ed) Techniques in rheological measurement. Springer, Dordrecht, pp 99–121

    Google Scholar 

  • Glagov S, Weisenberg E, Zarins CK, Stankunavicius R, Kolettis GJ (1987) Compensatory enlargement of human atherosclerotic coronary arteries. N Engl J Med 316(22):1371–1375

    Google Scholar 

  • Gutierrez-Chico JL, Zhao S, Chatzizisis YS (2018) Vorticity: at the crossroads of coronary biomechanics and physiology. Atherosclerosis 273:115–116

    Google Scholar 

  • Hatami J, Tafazzoli-Shadpour M, Haghighipour N, Shokrgozar MA, Janmaleki M (2013) Influence of cyclic stretch on mechanical properties of endothelial cells. Exp Mech 53(8):1291–1298

    Google Scholar 

  • Hennerici M, Aulich A, Sandmann W, Freund HJ (1981) Incidence of asymptomatic extracranial arterial disease. Stroke 12(6):750–758

    Google Scholar 

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

    Google Scholar 

  • Hoi Y, Zhou YQ, Zhang X, Henkelman RM, Steinman DA (2011) Correlation between local hemodynamics and lesion distribution in a novel aortic regurgitation murine model of atherosclerosis. Ann Biomed Eng 39(5):1414–1422

    Google Scholar 

  • Howard VJ, McClure LA, Meschia JF, Pulley L, Orr SC, Friday GH (2006) High prevalence of stroke symptoms among persons without a diagnosis of stroke or transient ischemic attack in a general population: the REasons for Geographic And Racial Differences in Stroke (REGARDS) study. Arch Intern Med 166(18):1952–1958

    Google Scholar 

  • Ku DN, Giddens DP (1983) Pulsatile flow in a model carotid bifurcation. Arterioscler Thromb Vasc Biol 3(1):31–39

    Google Scholar 

  • Langille BL, O’Donnell F (1986) Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. Science 231(4736):405–407

    Google Scholar 

  • Lee S-W, Antiga L, Steinman DA (2009) Correlations among indicators of disturbed flow at the normal carotid bifurcation. J Biomech Eng 131(6):061013

    Google Scholar 

  • Lehoux S, Jones EA (2016) Shear stress, arterial identity and atherosclerosis. Thromb Haemost 115(3):467–473

    Google Scholar 

  • Li Z, Xu X, Xia J, Deng X, Zeng T (2017) Quantitative evaluation between wall shear stress and artery angle in three-dimensional atherosclerotic carotid bifurcation model. J Med Imag Health Inform 7(4):805–809

    Google Scholar 

  • Linton MF, Yancey PG, Davies SS, Jerome WG, Linton EF, Song WL, Doran AC , Vickers KC (2019) The role of lipids and lipoproteins in atherosclerosis. Endotext [Internet], MDText. com, Inc.

  • Maurits N, Loots G, Veldman A (2007) The influence of vessel wall elasticity and peripheral resistance on the carotid artery flow wave form: a CFD model compared to in vivo ultrasound measurements. J Biomech 40(2):427–436

    Google Scholar 

  • Mazzi V, Gallo D, Calo K, Najafi M, Khan MO, De Nisco G, Steinman DA, Morbiducci U (2020) A Eulerian method to analyze wall shear stress fixed points and manifolds in cardiovascular flows. Biomech Model Mechanobiol 19(5):1403–1423

    Google Scholar 

  • Mendieta JB, Fontanarosa D, Wang J, Paritala PK, McGahan T, Lloyd T, Li Z (2020) The importance of blood rheology in patient-specific computational fluid dynamics simulation of stenotic carotid arteries. Biomech Model Mechanobiol 19(5):1477–1490

    Google Scholar 

  • Moore JE Jr (2009) Biomechanical issues in endovascular device design. J Endovasc Ther 16(Suppl 1):1–11

    Google Scholar 

  • Morbiducci U, Kok AM, Kwak BR, Stone PH, Steinman DA, Wentzel JJ (2016) Atherosclerosis at arterial bifurcations: evidence for the role of haemodynamics and geometry. Thromb Haemost 115(3):484–492

    Google Scholar 

  • Moyle KR, Antiga L, Steinman DA (2006) Inlet conditions for image-based CFD models of the carotid bifurcation: is it reasonable to assume fully developed flow? J Biomech Eng 128(3):371–379

    Google Scholar 

  • Nasu K, Tsuchikane E, Katoh O, Vince DG, Virmani R, Surmely JF, Murata A, Takeda Y, Ito T, Ehara M, Matsubara T, Terashima M, Suzuki T (2006) Accuracy of in vivo coronary plaque morphology assessment: a validation study of in vivo virtual histology compared with in vitro histopathology. J Am Coll Cardiol 47(12):2405–2412

    Google Scholar 

  • NIROOMANDOSCUII H, Tafazzoli-Shadpour M, Ghalichi F (2007) Biomechanical analysis of wall remodeling in elastic arteries with application of fluid–solid interaction methods. J Mech Med Biol 7(04):433–447

    Google Scholar 

  • Niu L, Meng L, Xu L, Liu J, Wang Q, Xiao Y, Qian M, Zheng H (2015) Stress phase angle depicts differences in arterial stiffness: phantom and in vivo study. Phys Med Biol 60(11):4281–4294

    Google Scholar 

  • Or S (1997) Do plaques grow upstream or downstream? An angiographic study in the femoral artery. Arterioscler Thromb Vasc Biol 17(5):912–918

    Google Scholar 

  • Peiffer V, Sherwin SJ, Weinberg PD (2013) Does low and oscillatory wall shear stress correlate spatially with early atherosclerosis? Syst Rev Cardiovasc Res 99(2):242–250

    Google Scholar 

  • Qiu Y, Tarbell JM (2000) Numerical simulation of pulsatile flow in a compliant curved tube model of a coronary artery. J Biomech Eng 122(1):77–85

    Google Scholar 

  • Razavi A, Shirani E, Sadeghi M (2011) Numerical simulation of blood pulsatile flow in a stenosed carotid artery using different rheological models. J Biomech 44(11):2021–2030

    Google Scholar 

  • Rezvani-Sharif A, Tafazzoli-Shadpour M, Avolio A (2019) Progressive changes of elastic moduli of arterial wall and atherosclerotic plaque components during plaque development in human coronary arteries. Med Biol Eng Comput 57(3):731–740

    Google Scholar 

  • Salzar RS, Thubrikar MJ, Eppink RT (1995) Pressure-induced mechanical stress in the carotid artery bifurcation: a possible correlation to atherosclerosis. J Biomech 28(11):1333–1340

    Google Scholar 

  • Samaee M, Tafazzoli-Shadpour M, Alavi H (2017) Coupling of shear–circumferential stress pulses investigation through stress phase angle in FSI models of stenotic artery using experimental data. Med Biol Eng Comput 55(8):1147–1162

    Google Scholar 

  • Selzer RH, Mack WJ, Lee PL, Kwong-Fu H, Hodis HN (2001) Improved common carotid elasticity and intima-media thickness measurements from computer analysis of sequential ultrasound frames. Atherosclerosis 154(1):185–193

    Google Scholar 

  • Sharma S, Singh U, Katiyar VK (2015) Magnetic field effect on flow parameters of blood along with magnetic particles in a cylindrical tube. J Magn Magn Mater 377:395–401

    Google Scholar 

  • Shoajei S, Tafazzoli-Shahdpour M, Shokrgozar MA, Haghighipour N (2014) Alteration of human umbilical vein endothelial cell gene expression in different biomechanical environments. Cell Biol Int 38(5):577–581

    Google Scholar 

  • Shojaei S, Tafazzoli-Shadpour M, Shokrgozar MA, Haghighipour N, Jahromi FH (2018) Stress phase angle regulates differentiation of human adipose-derived stem cells toward endothelial phenotype. Prog Biomater 7(2):121–131

    Google Scholar 

  • Stone PH, Saito S, Takahashi S, Makita Y, Nakamura S, Kawasaki T, Takahashi A, Katsuki T, Nakamura S, Namiki A (2012) Prediction of progression of coronary artery disease and clinical outcomes using vascular profiling of endothelial shear stress and arterial plaque characteristics: the PREDICTION Study. Circulation 126(2):172–181

    Google Scholar 

  • Suarez-Cunqueiro MM, Duker J, Liebehenschel N, Schon R, Schmelzeisen R (2002) Calcification of the branches of the external carotid artery detected by panoramic radiography: a case report. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 94(5):636–640

    Google Scholar 

  • Sugiyama S, Niizuma K, Nakayama T, Shimizu H, Endo H, Inoue T, Fujimura M, Ohta M, Takahashi A, Tominaga T (2013) Relative residence time prolongation in intracranial aneurysms: a possible association with atherosclerosis. Neurosurgery 73(5):767–776

    Google Scholar 

  • Tada S, Tarbell J (2005) A computational study of flow in a compliant carotid bifurcation–stress phase angle correlation with shear stress. Ann Biomed Eng 33(9):1202–1212

    Google Scholar 

  • Taghizadeh H, Tafazzoli-Shadpour M, Shadmehr MB (2015) Analysis of arterial wall remodeling in hypertension based on lamellar modeling. J Am Soc Hypertens 9(9):735–744

    Google Scholar 

  • Tang BT, Cheng CP, Draney MT, Wilson NM, Tsao PS, Herfkens RJ, Taylor CA (2006) Abdominal aortic hemodynamics in young healthy adults at rest and during lower limb exercise: quantification using image-based computer modeling. Am J Physiol Heart Circ Physiol 291(2):H668-676

    Google Scholar 

  • Tang D, Yang C, Mondal S, Liu F, Canton G, Hatsukami TS, Yuan C (2008) A negative correlation between human carotid atherosclerotic plaque progression and plaque wall stress: In vivo MRI-based 2D/3D FSI models. J Biomech 41(4):727–736

    Google Scholar 

  • Taylor CA, Hughes TJ, Zarins CK (1998) Finite element modeling of three-dimensional pulsatile flow in the abdominal aorta: relevance to atherosclerosis. Ann Biomed Eng 26(6):975–987

    Google Scholar 

  • Thomas JB, Antiga L, Che SL, Milner JS, Steinman DA, Spence JD, Rutt BK, Steinman DA (2005) Variation in the carotid bifurcation geometry of young versus older adults: implications for geometric risk of atherosclerosis. Stroke 36(11):2450–2456

    Google Scholar 

  • Yamamoto E, Siasos G, Zaromytidou M, Coskun AU, Xing L, Bryniarski K, Zanchin T, Sugiyama T, Lee H, Stone PH, Jang IK (2017) Low endothelial shear stress predicts evolution to high-risk coronary plaque phenotype in the future: a serial optical coherence tomography and computational fluid dynamics study. Circ Cardiovasc Interv 10(8):e005455

    Google Scholar 

  • Yang C, Canton G, Yuan C, Ferguson M, Hatsukami TS, Tang D (2010a) Advanced human carotid plaque progression correlates positively with flow shear stress using follow-up scan data: an in vivo MRI multi-patient 3D FSI study. J Biomech 43(13):2530–2538

    Google Scholar 

  • Yang C, Canton G, Yuan C, Ferguson M, Hatsukami TS, Tang D (2010b) Advanced human carotid plaque progression correlates positively with flow shear stress using follow-up scan data: An< i> in vivo</i> MRI multi-patient 3D FSI study. J Biomech 43(13):2530–2538

    Google Scholar 

  • Yang S, Wang Q, Shi W, Guo W, Jiang Z, Gong X (2019) Numerical study of biomechanical characteristics of plaque rupture at stenosed carotid bifurcation: a stenosis mechanical property-specific guide for blood pressure control in daily activities. Acta Mech Sin 35(6):1279–1289

    Google Scholar 

  • Yousif MY, Holdsworth DW, Poepping TL (2010) A blood-mimicking fluid for particle image velocimetry with silicone vascular models. Exp Fluids 50(3):769–774

    Google Scholar 

  • Zarins CK, Giddens DP, Bharadvaj B, Sottiurai VS, Mabon RF, Glagov S (1983) Carotid bifurcation atherosclerosis Quantitative correlation of plaque localization with flow velocity profiles and wall shear stress. Circul Res 53(4):502–514

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Cardiovascular Engineering Lab, Faculty of Biomedical Engineering, Amirkabir University of Technology, Tehran, Iran

    Mahyar Ahmadpour-B & Mohammad Tafazzoli-Shadpour

  2. Tissue Mechanics Lab, Faculty of Biomedical Engineering, Sahand University of Technology, Tabriz, Iran

    Ahmad Nooraeen & Hadi Taghizadeh

Authors
  1. Mahyar Ahmadpour-B
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ahmad Nooraeen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohammad Tafazzoli-Shadpour
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hadi Taghizadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Mohammad Tafazzoli-Shadpour or Hadi Taghizadeh.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahmadpour-B, M., Nooraeen, A., Tafazzoli-Shadpour, M. et al. Contribution of atherosclerotic plaque location and severity to the near-wall hemodynamics of the carotid bifurcation: an experimental study and FSI modeling. Biomech Model Mechanobiol 20, 1069–1085 (2021). https://doi.org/10.1007/s10237-021-01431-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-021-01431-x

Keywords

Search

Navigation