The paper deals with the impact of chosen geometric and material factors on maximal stresses in carotid atherosclerotic plaque calculated using patient-specific finite element models. These stresses are believed to be decisive for the plaque vulnerability but all applied models suffer from inaccuracy of input data, especially when obtained in vivo only. One hundred computational models based on ex vivo MRI are used to investigate the impact of wall thickness, MRI slice thickness, lipid core and fibrous tissue stiffness, and media anisotropy on the calculated peak plaque and peak cap stresses. The investigated factors are taken as continuous in the range based on published experimental results, only the impact of anisotropy is evaluated by comparison with a corresponding isotropic model. Design of Experiment concept is applied to assess the statistical significance of these investigated factors representing uncertainties in the input data of the model. The results show that consideration of realistic properties of arterial wall in the model is decisive for the stress evaluation; assignment of properties of fibrous tissue even to media and adventitia layers as done in some studies may induce up to eightfold overestimation of peak stress. The impact of MRI slice thickness may play a key role when local thin fibrous cap is present. Anisotropy of media layer is insignificant, and the stiffness of fibrous tissue and lipid core may become significant in some combinations.

1st Department of Pathology St Anne's University Hospital Brno and Faculty of Medicine Masaryk University Brno Czech Republic

2nd Department of Surgery St Anne's University Hospital Brno and Faculty of Medicine Masaryk University Brno Czech Republic

Institute of Scientific Instruments The Czech Academy of Science Brno Czech Republic

Institute of Solid Mechanics Mechatronics and Biomechanics Brno University of Technology Brno Czech Republic

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Ross R. Inflammation or Atherogenesis. N Engl J Med. 1999;340: 115–126. PubMed

Finn A V., Nakano M, Narula J, Kolodgie FD, Virmani R. Concept of vulnerable/unstable plaque. Arterioscler Thromb Vasc Biol. 2010;30: 1282–1292. 10.1161/ATVBAHA.108.179739 PubMed DOI

Fisher M, Paganini-Hill A, Martin A, Cosgrove M, Toole JF, Barnett HJM, et al. Carotid plaque pathology: Thrombosis, ulceration, and stroke pathogenesis. Stroke. 2005;36: 253–257. 10.1161/01.STR.0000152336.71224.21 PubMed DOI

Akyildiz AC, Speelman L, van Brummelen H, Gutiérrez MA, Virmani R, van der Lugt A, et al. Effects of intima stiffness and plaque morphology on peak cap stress. Biomed Eng Online. 2011;10: 1–13. PubMed PMC

Maldonado N, Kelly-Arnold A, Vengrenyuk Y, Laudier D, Fallon JT, Virmani R, et al. A mechanistic analysis of the role of microcalcifications in atherosclerotic plaque stability: potential implications for plaque rupture. AJP Hear Circ Physiol. 2012;303: H619–H628. 10.1152/ajpheart.00036.2012 PubMed DOI PMC

Nieuwstadt HA, Akyildiz AC, Speelman L, Virmani R, van der Lugt A, van der Steen AFW, et al. The influence of axial image resolution on atherosclerotic plaque stress computations. J Biomech. 2013;46: 689–695. 10.1016/j.jbiomech.2012.11.042 PubMed DOI

Yuan J, Teng Z, Feng J, Zhang Y, Brown AJ, Gillard JH, et al. Influence of material property variability on the mechanical behaviour of carotid atherosclerotic plaques: A 3D fluid-structure interaction analysis. Int j numer method biomed eng. 2015. 10.1002/cnm.2722 PubMed DOI PMC

Holzapfel GA, Stadler M, Schulze-Bauer CAJ. A Layer-Specific Three-Dimensional Model for the Simulation of Balloon Angioplasty using Magnetic Resonance Imaging and Mechanical Testing. Ann Biomed Eng. 2002;30: 753–767. 10.1114/1.1492812 PubMed DOI

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

Huang Y, Teng Z, Sadat U, Graves MJ, Bennett MR, Gillard JH. The influence of computational strategy on prediction of mechanical stress in carotid atherosclerotic plaques: Comparison of 2D structure-only, 3D structure-only, one-way and fully coupled fluid-structure interaction analyses. J Biomech. 2014;47: 1465–1471. 10.1016/j.jbiomech.2014.01.030 PubMed DOI PMC

Cilla M, Borrás I, Peña E, Martínez MA, Malvè M. A parametric model for analysing atherosclerotic arteries: On the FSI coupling. Int Commun Heat Mass Transf. 2015;67: 29–38. 10.1016/j.icheatmasstransfer.2015.06.017 DOI

Tang D, Yang C, Huang S, Mani V, Zheng J, Woodard PK, et al. Cap inflammation leads to higher plaque cap strain and lower cap stress: An MRI-PET/CT-based FSI modeling approach. J Biomech. 2017;50: 121–129. 10.1016/j.jbiomech.2016.11.011 PubMed DOI PMC

Akyildiz AC, Speelman L, Gijsen FJH. Mechanical properties of human atherosclerotic intima tissue. J Biomech. 2014;47: 773–783. 10.1016/j.jbiomech.2014.01.019 PubMed DOI

Walsh MT, Cunnane EM, Mulvihill JJ, Akyildiz AC, Gijsen FJH, Holzapfel GA. Uniaxial tensile testing approaches for characterisation of atherosclerotic plaques. J Biomech. 2014;47: 793–804. 10.1016/j.jbiomech.2014.01.017 PubMed DOI

Huang X, Yang C, Zheng J, Bach R, Muccigrosso D, Woodard PK, et al. 3D MRI-based multicomponent thin layer structure only plaque models for atherosclerotic plaques. J Biomech. 2016;49: 2726–2733. 10.1016/j.jbiomech.2016.06.002 PubMed DOI PMC

Iannaccone F, Debusschere N, De Bock S, De Beule M, Van Loo D, Vermassen F, et al. The influence of vascular anatomy on carotid artery stenting: A parametric study for damage assessment. J Biomech. 2014;47: 890–898. 10.1016/j.jbiomech.2014.01.008 PubMed DOI

Sommer G, Regitnig P, Koltringer L, Holzapfel GA. Biaxial mechanical properties of intact and layer-dissected human carotid arteries at physiological and supraphysiological loadings. AJP Hear Circ Physiol. 2010;298: H898–H912. 10.1152/ajpheart.00378.2009 PubMed DOI

Kamenskiy A V., Dzenis YA, Kazmi SAJ, Pemberton MA, Pipinos II, Phillips NY, et al. Biaxial mechanical properties of the human thoracic and abdominal aorta, common carotid, subclavian, renal and common iliac arteries. Biomech Model Mechanobiol. 2014;13: 1341–1359. 10.1007/s10237-014-0576-6 PubMed DOI

Loree HM, Kamm RD, Stringfellow RG, Lee RT. Effects of Fibrous Cap Thickness on Peak Circumferential Stress in Model Atherosclerotic Vessels. Circulation. 1992;71: 850–858. PubMed

Holzapfel GA, Mulvihill JJ, Cunnane EM, Walsh MT. Computational approaches for analyzing the mechanics of atherosclerotic plaques: A review. J Biomech. 2014;47: 859–869. 10.1016/j.jbiomech.2014.01.011 PubMed DOI

Cilla M, Peña E, Martínez MA. 3D computational parametric analysis of eccentric atheroma plaque: Influence of axial and circumferential residual stresses. Biomech Model Mechanobiol. 2012;11: 1001–1013. 10.1007/s10237-011-0369-0 PubMed DOI

Groen HC, Van Walsum T, Rozie S, Klein S, Van Gaalen K, Gijsen FJH, et al. Three-dimensional registration of histology of human atherosclerotic carotid plaques to in-vivo imaging. J Biomech. 2010;43: 2087–2092. 10.1016/j.jbiomech.2010.04.005 PubMed DOI

Stary HC. Natural History and Histological Classification of Atherosclerotic Lesions. Aterioscler Thromb Vasc Biol. 2000;20: 1177–1178. PubMed

Lisický O, Malá A, Burša J. Influence of Transversal Resolution on Reconstructing Atherosclerotic Plaque Components. VipIMAGE 2019. 2019. pp. 501–508.

Sommer G, Holzapfel GA. 3D constitutive modeling of the biaxial mechanical response of intact and layer-dissected human carotid arteries. J Mech Behav Biomed Mater. 2012;5: 116–128. 10.1016/j.jmbbm.2011.08.013 PubMed DOI

Holzapfel GA, Sommer G, Gasser CT, Regitnig P. Determination of layer-specific mechanical properties of human coronary arteries with nonatherosclerotic intimal thickening and related constitutive modeling. J Physiol Hear Circ Physiol. 2005;103: 806–808. 10.1152/ajpheart.00934.2004 PubMed DOI

Holzapfel GA, Sommer G, Regitnig P. Anisotropic Mechanical Properties of Tissue Components in Human Atherosclerotic Plaques. J Biomech Eng. 2004;126: 657 10.1115/1.1800557 PubMed DOI

Yeoh OH. Some forms of the strain energy function for rubber. Rubber Chemistry and Technology. 1993. pp. 754–771.

Marcián P, Narra N, Borák L, Chamrad J, Wolff J. Biomechanical performance of cranial implants with different thicknesses and material properties: A finite element study. Comput Biol Med. 2019;109: 43–52. 10.1016/j.compbiomed.2019.04.016 PubMed DOI

Libby P, Pasterkamp G. Requiem for the “vulnerable plaque.” Eur Heart J. 2015;36: 2984–2987. 10.1093/eurheartj/ehv349 PubMed DOI

Burke F. CORONARY RISK FACTORS AND PLAQUE MORPHOLOGY IN MEN WITH CORONARY DISEASE WHO DIED SUDDENLY. New Engl J Med Coron. 1997. PubMed

Hatsukami TS, Ross R, Polissar NL, Yuan C. Visualization of fibrous cap thickness and rupture in human atherosclerotic carotid plaque in vivo with high-resolution magnetic resonance imaging. Circulation. 2000;102: 959–964. 10.1161/01.cir.102.9.959 PubMed DOI

Saam T, Ferguson MS, Yarnykh VL, Takaya N, Xu D, Polissar NL, et al. Quantitative evaluation of carotid plaque composition by in vivo MRI. Arterioscler Thromb Vasc Biol. 2005;25: 234–239. 10.1161/01.ATV.0000149867.61851.31 PubMed DOI

Maldonado N, Kelly-Arnold A, Laudier D, Weinbaum S, Cardoso L. Imaging and analysis of microcalcifications and lipid/necrotic core calcification in fibrous cap atheroma. Int J Cardiovasc Imaging. 2015;31: 1079–1087. 10.1007/s10554-015-0650-x PubMed DOI PMC

Kiousis DE, Rubinigg SF, Auer M, Holzapfel GA. 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. 2009;131: 121002 10.1115/1.4000078 PubMed DOI

Holzapfel Gerhard A. ORW. A New Constitutive Framework for Arterial Wall Mechanics and a Comparative Study of Material Models. J Elast. 2000;61: 1–48. 10.1023/A:1010835316564 DOI

Gasser TC, Ogden RW, Holzapfel GA. Hyperelastic modelling of arterial layers with distributed collagen fibre orientations. J R Soc Interface. 2005;3: 15–35. 10.1098/rsif.2005.0073 PubMed DOI PMC

Holzapfel GA, Ogden RW. Biomechanical relevance of the microstructure in artery walls with a focus on passive and active components. Am J Physiol—Hear Circ Physiol. 2018;315: H540–H549. 10.1152/ajpheart.00117.2018 PubMed DOI

Zobrazit více v PubMed

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