Skip to main content

Advertisement

SpringerLink
Log in

Prediction of fibre architecture and adaptation in diseased carotid bifurcations

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

Abstract

Many studies have used patient-specific finite element models to estimate the stress environment in atherosclerotic plaques, attempting to correlate the magnitude of stress to plaque vulnerability. In complex geometries, few studies have incorporated the anisotropic material response of arterial tissue. This paper presents a fibre remodelling algorithm to predict the fibre architecture, and thus anisotropic material response in four patient-specific models of the carotid bifurcation. The change in fibre architecture during disease progression and its affect on the stress environment in the plaque were predicted. The mean fibre directions were assumed to lie at an angle between the two positive principal strain directions. The angle and the degree of dispersion were assumed to depend on the ratio of principal strain values. Results were compared with experimental observations and other numerical studies. In non-branching regions of each model, the typical double helix arterial fibre pattern was predicted while at the bifurcation and in regions of plaque burden, more complex fibre architectures were found. The predicted change in fibre architecture in the arterial tissue during plaque progression was found to alter the stress environment in the plaque. This suggests that the specimen-specific anisotropic response of the tissue should be taken into account to accurately predict stresses in the plaque. Since determination of the fibre architecture in vivo is a difficult task, the system presented here provides a useful method of estimating the fibre architecture in complex arterial geometries.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Alastrue V, Garcia A, Pena E, Rodriguez JF, Martinez MA, Doblare M (2010) Numerical framework for patient-specific computational modelling of vascular tissue. Int J Numer Meth Bio 26(1): 35–51

    Article  MATH  Google Scholar 

  • Ateshian GA (2007) Anisotropy of fibrous tissues in relation to the distribution of tensed and buckled fibers. J Biomech Eng 129(2): 240–249. doi:10.1115/1.2486179

    Article  Google Scholar 

  • Cheng GC, Loree HM, Kamm RD, Fishbein MC, Lee RT (1993) Distribution of circumferential stress in ruptured and stable atherosclerotic lesions. A structural analysis with histopathological correlation. Circulation 87(4): 1179–1187

    Google Scholar 

  • Creane A, Maher E, Sultan S, Hynes N, Kelly DJ, Lally C (2010) Finite element modelling of diseased carotid bifurcations generated from in vivo computerised tomographic angiography. Comput Biol Med 40(4): 419–429. doi:10.1016/j.compbiomed.2010.02.006

    Article  Google Scholar 

  • Delfino A, Stergiopulos N, Moore JE Jr, Meister JJ (1997) Residual strain effects on the stress field in a thick wall finite element model of the human carotid bifurcation. J Biomech 30(8): 777–786. doi:S0021929097000250 [pii]

    Article  Google Scholar 

  • Driessen NJB, Bouten CVC, Baaijens FPT (2005) Improved prediction of the collagen fiber architecture in the aortic heart valve. J Biomech Eng T Asme 127(2): 329–336. doi:10.1115/1.1865187

    Article  Google Scholar 

  • Driessen NJB, Cox MAJ, Bouten CVC, Baaijens FPT (2008) Remodelling of the angular collagen fiber distribution in cardiovascular tissues. Biomech Model Mechan 7(2): 93–103. doi:10.1007/s10237-007-0078-x

    Article  Google Scholar 

  • Driessen NJB, Wilson W, Bouten CVC, Baaijens FPT (2004) A computational model for collagen fibre remodelling in the arterial wall. J Theor Biol 226(1): 53–64. doi:10.1016/j.jtbi.2003.08.004

    Article  Google Scholar 

  • Finlay HM, Whittaker P, Canham PB (1998) Collagen organization in the branching region of human brain arteries. Stroke 29(8): 1595–1601

    Article  Google Scholar 

  • Flamini V, Kerskens C, Moerman KM, Simms CK, Lally C (2010) Imaging arterial fibres using diffusion tensor imaging-feasibility study and preliminary results. Eurasip J Adv Sig Pr. doi:10.1155/2010/904091

  • Freed AD (2008) Anisotropy in hypoelastic soft-tissue mechanics, i: theory. J Mech Mater Struct 3(5): 911–928

    Article  MathSciNet  Google Scholar 

  • Freed AD, Einstein DR, Vesely I (2005) Invariant formulation for dispersed transverse isotropy in aortic heart valves—an efficient means for modeling fiber splay. Biomech Model Mechan 4(2-3): 100–117. doi:10.1007/s10237-005-0069-8

    Article  Google Scholar 

  • Gao H, Long Q (2008) Effects of varied lipid core volume and fibrous cap thickness on stress distribution in carotid arterial plaques. J Biomech 41(14): 3053–3059. doi:10.1016/j.jbiomech.2008.07.011

    Article  Google Scholar 

  • Gao H, Long Q, Graves M, Gillard JH, Li ZY (2009) Carotid arterial plaque stress analysis using fluid-structure interactive simulation based on in-vivo magnetic resonance images of four patients. J Biomech 42(10): 1416–1423. doi:10.1016/j.jbiomech.2009.04.010

    Article  Google Scholar 

  • Gasser TC, Ogden RW, Holzapfel GA (2006) Hyperelastic modelling of arterial layers with distributed collagen fibre orientations. J R Soc Interface 3(6): 15–35. doi:10.1098/rsif.2005.0073

    Article  Google Scholar 

  • Glagov S, Zarins C, Giddens DP, Ku DN (1988) Hemodynamics and atherosclerosis. Insights and perspectives gained from studies of human arteries. Arch Pathol Lab Med 112(10): 1018–1031

    Google Scholar 

  • Grytz R, Meschke G (2010) A computational remodeling approach to predict the physiological architecture of the collagen fibril network in corneo-scleral shells. Biomech Model Mechanobiol 9(2): 225–235. doi:10.1007/s10237-009-0173-2

    Article  Google Scholar 

  • Grytz R, Meschke G, Jonas JB (2010) The collagen fibril architecture in the lamina cribrosa and peripapillary sclera predicted by a computational remodeling approach. Biomech Model Mechanobiol. doi:10.1007/s10237-010-0240-8

  • Hardie AD, Kramer CM, Raghavan P, Baskurt E, Nandalur KR (2007) The impact of expansive arterial remodeling on clinical presentation in carotid artery disease: a multidetector ct angiography study. Am J Neuroradiol 28(6): 1067–1070. doi:10.3174/Ajnr.A0508

    Article  Google Scholar 

  • Hariton I, deBotton G, Gasser TC, Holzapfel GA (2007a) Stress-driven collagen fiber remodeling in arterial walls. Biomech Model Mechanobiol 6(3): 163–175. doi:10.1007/s10237-006-0049-7

    Article  Google Scholar 

  • Hariton I, deBotton G, Gasser TC, Holzapfel GA (2007b) Stress-modulated collagen fiber remodeling in a human carotid bifurcation. J Theor Biol 248(3): 460–470. doi:10.1016/j.jtbi.2007.05.037

    Article  Google Scholar 

  • Hayashi K, Mani V, Nemade A, Aguiar S, Postley JE, Fuster V, Fayad ZA (2010) Variations in atherosclerosis and remodeling patterns in aorta and carotids. J Cardiovasc Magn R 12: 10. doi:10.1186/1532-429x-12-10

    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 61(1–3): 1–48

    Article  MathSciNet  MATH  Google Scholar 

  • Holzapfel GA, Gasser TC, Stadler M (2002) A structural model for the viscoelastic behavior of arterial walls: continuum formulation and finite element analysis. Eur J Mech A Solids 21(3): 441–463. doi:10.1016/s0997-7538(01)01206-2

    Article  MATH  Google Scholar 

  • Holzapfel GA, Ogden RW (2010) Constitutive modelling of arteries. P Roy Soc A Math Phy 466(2118): 1551–1596. doi:10.1098/rspa.2010.0058

    Article  MathSciNet  MATH  Google Scholar 

  • Humphrey JD, Eberth JF, Dye WW, Gleason RL (2009) Fundamental role of axial stress in compensatory adaptations by arteries. J Biomech 42(1): 1–8. doi:10.1016/j.jbiomech.2008.11.011

    Article  Google Scholar 

  • Kingsley PB (2006) Introduction to diffusion tensor imaging mathematics: part i. Tensors, rotations, and eigenvectors. Concepts Magn Reson Part A 28A(2): 101–122. doi:10.1002/cmr.a.20048

    Article  Google Scholar 

  • Kiousis DE, Rubinigg SF, Auer M, Holzapfel GA (2009) A methodology to analyze changes in lipid core and calcification onto fibrous cap vulnerability: the human atherosclerotic carotid bifurcation as an illustratory example. J Biomech Eng 131(12): 121002. doi:10.1115/1.4000078

    Article  Google Scholar 

  • Kuhl E, Holzapfel GA (2007) A continuum model for remodeling in living structures. J Mater Sci 42(21): 8811–8823. doi:10.1007/s10853-007-1917-y

    Article  Google Scholar 

  • Li ZY, Howarth S, Trivedi RA, JM UK-I, Graves MJ, Brown A, Wang L, Gillard JH (2006) Stress analysis of carotid plaque rupture based on in vivo high resolution mri. J Biomech 39(14): 2611–2622. doi:10.1016/j.jbiomech.2005.08.022

    Article  Google Scholar 

  • Li ZY, Howarth SP, Tang T, Graves MJ, J UK-I, Trivedi RA, Kirkpatrick PJ, Gillard JH (2007) Structural analysis and magnetic resonance imaging predict plaque vulnerability: a study comparing symptomatic and asymptomatic individuals. J Vasc Surg 45(4): 768–775. doi:10.1016/j.jvs.2006.12.065

    Article  Google Scholar 

  • Maher E, Creane A, Sultan S, Hynes N, Lally C, Kelly DJ (2009) Tensile and compressive properties of fresh human carotid atherosclerotic plaques. J Biomech 42(16): 2760–2767. doi:10.1016/j.jbiomech.2009.07.032

    Article  Google Scholar 

  • Miehe C (1996) Numerical computation of algorithmic (consistent) tangent moduli in large-strain computational inelasticity. Comput Method Appl M 134(3–4): 223–240

    Article  MATH  Google Scholar 

  • Mortier P, Holzapfel GA, De Beule M, Van Loo D, Taeymans Y, Segers P, Verdonck P, Verhegghe B (2010) A novel simulation strategy for stent insertion and deployment in curved coronary bifurcations: comparison of three drug-eluting stents. Ann Biomed Eng 38(1): 88–99. doi:10.1007/s10439-009-9836-5

    Article  Google Scholar 

  • Nagel T, Kelly DJ (2010) Mechano-regulation of mesenchymal stem cell differentiation and collagen organisation during skeletal tissue repair. Biomech Model Mech 9(3): 359–372. doi:10.1007/s10237-009-0182-1

    Article  Google Scholar 

  • O’Connell MK, Murthy S, Phan S, Xu C, Buchanan J, Spilker R, Dalman RL, Zarins CK, Denk W, Taylor CA (2008) The three-dimensional micro- and nanostructure of the aortic medial lamellar unit measured using 3d confocal and electron microscopy imaging. Matrix Biol 27(3): 171–181. doi:10.1016/j.matbio.2007.10.008

    Article  Google Scholar 

  • Patel DJ, Janicki JS, Carew TE (1969) Static anisotropic elastic properties of aorta in living dogs. Circ Res 25(6): 765–779

    Google Scholar 

  • Pierce DM, Trobin W, Raya JG, Trattnig S, Bischof H, Glaser C, Holzapfel GA (2010) Dt-mri based computation of collagen fiber deformation in human articular cartilage: a feasibility study. Ann Biomed Eng 38(7): 2447–2463. doi:10.1007/s10439-010-9990-9

    Article  Google Scholar 

  • Rhodin JAG (1980) Architecture of the vessel wall. In: Sparks HV, Bohr DF, Somlyo AD, Geiger SR (eds) Handbook of physiology, the cardiovascular system. American Physiological Society, Bethesda, pp 1–31

    Google Scholar 

  • Rodriguez JF, Ruiz C, Doblare M, Holzapfel GA (2008) Mechanical stresses in abdominal aortic aneurysms: influence of diameter, asymmetry, and material anisotropy. J Biomech Eng 130(2): 021023. doi:10.1115/1.2898830

    Article  Google Scholar 

  • Rowe AJ, Finlay HM, Canham PB (2003) Collagen biomechanics in cerebral arteries and bifurcations assessed by polarizing microscopy. J Vasc Res 40(4): 406–415. doi:10.1159/000072831

    Article  Google Scholar 

  • Sun W, Chaikof EL, Levenston ME (2008) Numerical approximation of tangent moduli for finite element implementations of nonlinear hyperelastic material models. J Biomech Eng 130(6): 061003. doi:10.1115/1.2979872

    Article  Google Scholar 

  • Taber LA, Humphrey JD (2001) Stress-modulated growth, residual stress, and vascular heterogeneity. J Biomech Eng 123(6): 528–535

    Article  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. doi:10.1016/j.jbiomech.2007.11.026

    Article  Google Scholar 

  • Wilson W, Driessen NJ, van Donkelaar CC, Ito K (2006) Prediction of collagen orientation in articular cartilage by a collagen remodeling algorithm. Osteoarthr Cartil 14(11): 1196–1202. doi:10.1016/j.joca.2006.05.006

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Mechanical and Manufacturing Engineering, Dublin City University, Dublin 9, Ireland

    Arthur Creane & Caitríona Lally

  2. Trinity Centre for Bioengineering, School of Engineering, Trinity College, Dublin 2, Ireland

    Eoghan Maher, Daniel J. Kelly & Caitríona Lally

  3. Western Vascular Institute, Department of Vascular & Endovascular Surgery, University College Hospital Galway, Galway, Ireland

    Sherif Sultan & Niamh Hynes

  4. Department of Vascular and Endovascular Surgery, Galway Clinic, Doughiska, Dublin Road, Galway, Ireland

    Sherif Sultan & Niamh Hynes

Authors
  1. Arthur Creane
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eoghan Maher
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sherif Sultan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Niamh Hynes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Daniel J. Kelly
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Caitríona Lally
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Caitríona Lally.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Creane, A., Maher, E., Sultan, S. et al. Prediction of fibre architecture and adaptation in diseased carotid bifurcations. Biomech Model Mechanobiol 10, 831–843 (2011). https://doi.org/10.1007/s10237-010-0277-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-010-0277-8

Keywords

Search

Navigation