Material properties of components in human carotid atherosclerotic plaques: A uniaxial extension study

Acta Biomaterialia

Volumn 10, Issue 12, 2014, Pages 5055-5063

  Teng, Zhongzhao ^a,b   Zhang, Yongxue ^a,c   Huang, Yuan ^a   Feng, Jiaxuan ^c   Yuan, Jianmin ^a   Lu, Qingsheng ^c   Sutcliffe, Michael P F ^b   Brown, Adam J ^d   Jing, Zaiping ^c   Gillard, Jonathan H ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c SECOND MILITARY MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Atherosclerosis; Haemorrhage; Lipid; Material property; Thrombus

Indexed keywords

BIOMECHANICS; ELASTIC MODULI; STRAIN ENERGY; TISSUE;

ATHEROSCLEROTIC PLAQUE; CAROTID PLAQUES; COMPUTATIONAL MODELLING; HAEMORRAGE; ITS APPLICATIONS; MECHANICAL LOADING; MEDIAN VALUE; STRAIN ENERGY DENSITY FUNCTIONS; STRESSES RELATIONSHIP; UNIAXIAL EXTENSION;

HISTOLOGY;

CALCIUM; LIPID;

AGED; ARTICLE; BLEEDING; CAROTID ATHEROSCLEROSIS; CAROTID ENDARTERECTOMY; CLINICAL ARTICLE; FEMALE; HUMAN; HUMAN TISSUE; INTRAPLAQUE HAEMORRHAGE; INTRAPLAQUE THROMBUS; MALE; MATERIALS TESTING; MATHEMATICAL MODEL; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RIGIDITY; THROMBUS; YOUNG MODULUS; BIOLOGICAL MODEL; CAROTID ARTERY; CAROTID ARTERY OBSTRUCTION; COMPUTER SIMULATION; IN VITRO STUDY; MECHANICAL STRESS; PATHOPHYSIOLOGY; SHEAR STRENGTH; TENSILE STRENGTH;

CAROTID ARTERIES; CAROTID STENOSIS; COMPUTER SIMULATION; ELASTIC MODULUS; HUMANS; IN VITRO TECHNIQUES; MODELS, CARDIOVASCULAR; SHEAR STRENGTH; STRESS, MECHANICAL; TENSILE STRENGTH;

EID: 84926365525     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.09.001     Document Type: Article

References (44)

1. WHO. The Global Burden of Disease: 2004 update. Geneva: WHO; 2008.
2. Levy EI, Mocco J, Samuelson RM, Ecker RD, Jahromi BS, Hopkins LN. Optimal treatment of carotid artery disease. J Am Coll Cardiol 2008; 51: 979-85.
3. Barnett HJ, Taylor DW, Eliasziw M, Fox AJ, Ferguson GG, Haynes RB, et al. Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med 1998; 339: 1415-25.
4. Rothwell PM, Gutnikov SA, Warlow CP. Reanalysis of the final results of the European Carotid Surgery Trial. Stroke 2003; 34: 514-23.
5. Yuan C, Zhang SX, Polissar NL, Echelard D, Ortiz G, Davis JW, et al. Identification of fibrous cap rupture with magnetic resonance imaging is highly associated with recent transient ischemic attack or stroke. Circulation 2002; 105: 181-5.
6. Chu B, Kampschulte A, Ferguson MS, Kerwin WS, Yarnykh VL, O'Brien KD, et al. Hemorrhage in the atherosclerotic carotid plaque: a high-resolution MRI study. Stroke 2004; 35: 1079-84.
7. Sadat U, Weerakkody RA, Bowden DJ, Young VE, Graves MJ, Li ZY, et al. Utility of high resolution MR imaging to assess carotid plaque morphology: a comparison of acute symptomatic, recently symptomatic and asymptomatic patients with carotid artery disease. Atherosclerosis 2009; 207: 434-9.
8. Eliasziw M, Streifler JY, Fox AJ, Hachinski VC, Ferguson GG, Barnett HJ. Significance of plaque ulceration in symptomatic patients with high-grade carotid stenosis. North American Symptomatic Carotid Endarterectomy Trial. Stroke 1994; 25: 304-8.
9. Altaf N, Daniels L, Morgan PS, Auer D, MacSweeney ST, Moody AR, et al. Detection of intraplaque hemorrhage by magnetic resonance imaging in symptomatic patients with mild to moderate carotid stenosis predicts recurrent neurological events. J Vasc Surg 2008; 47: 337-42.
10. Takaya N, Yuan C, Chu B, Saam T, Underhill H, Cai J, et al. Association between carotid plaque characteristics and subsequent ischemic cerebrovascular events: a prospective assessment with MRI - initial results. Stroke 2006; 37: 818-23.
11. Singh N, Moody AR, Gladstone DJ, Leung G, Ravikumar R, Zhan J, et al. Moderate carotid artery stenosis: MR imaging-depicted intraplaque hemorrhage predicts risk of cerebrovascular ischemic events in asymptomatic men. Radiology 2009; 252: 502-8.
12. Gao P, Chen ZQ, Bao YH, Jiao LQ, Ling F. Correlation between carotid intraplaque hemorrhage and clinical symptoms: systematic review of observational studies. Stroke 2007; 38: 2382-90.
13. Saam T, Hetterich H, Hoffmann V, Yuan C, Dichgans M, Poppert H, et al. Metaanalysis and systematic review of the predictive value of carotid plaque hemorrhage on cerebrovascular events by magnetic resonance imaging. J Am Coll Cardiol 2013; 62: 1081-91.
14. Milei J, Parodi JC, Ferreira M, Barrone A, Grana DR, Matturri L. Atherosclerotic plaque rupture and intraplaque hemorrhage do not correlate with symptoms in carotid artery stenosis. J Vasc Surg 2003; 38: 1241-7.
15. Teng Z, Sadat U, Huang Y, Young VE, Graves MJ, Lu J, et al. In vivo MRI-based 3D mechanical stress-strain profiles of carotid plaques with juxtaluminal plaque haemorrhage: an exploratory study for the mechanism of subsequent cerebrovascular events. Eur J Vasc Endovasc Surg 2011; 42: 427-33.
16. Teng Z, Sadat U, Brown AJ, Gillard JH. Plaque haemorrhage in carotid artery disease; pathogenesis, clinical and biomechanical considerations. J Biomech 2014; 47: 847-58.
17. Sadat U, Teng Z, Young VE, Walsh SR, Li ZY, Graves MJ, et al. Association between biomechanical structural stresses of atherosclerotic carotid plaques and subsequent ischaemic cerebrovascular events - a longitudinal in vivo magnetic resonance imaging-based finite element study. Eur J Vasc Endovasc Surg 2010.
18. U-King-Im JM, Young V, Gillard JH. Carotid-artery imaging in the diagnosis and management of patients at risk of stroke. Lancet Neurol 2009; 8: 569-80.
19. Cheng GC, Loree HM, Kamm RD, Fishbein MC, Lee RT. Distribution of circumferential stress in ruptured and stable atherosclerotic lesions. A structural analysis with histopathological correlation. Circulation 1993; 87: 1179-87.
20. Li ZY, Howarth S, Trivedi RA, UK-I JM, Graves MJ, Brown A, et al. Stress analysis of carotid plaque rupture based on in vivo high resolution MRI. J Biomech 2006; 39: 2611-22.
21. Sadat U, Li ZY, Graves MJ, Tang TY, Gillard JH. Noninvasive imaging of atheromatous carotid plaques. Nat Clin Pract 2009; 6: 200-9.
22. Richardson PD, Davies MJ, Born GV. Influence of plaque configuration and stress distribution on fissuring of coronary atherosclerotic plaques. Lancet 1989; 2: 941-4.
23. Sadat U, Li ZY, Young VE, Graves MJ, Boyle JR, Warburton EA, et al. Finite element analysis of vulnerable atherosclerotic plaques: a comparison of mechanical stresses within carotid plaques of acute and recently symptomatic patients with carotid artery disease. J Neurol Neurosurg Psychiatry 2010; 81: 286-9.
24. Zhu C, Teng Z, Sadat U, Young VE, Graves MJ, Li ZY, et al. Normalized wall index specific and MRI-based stress analysis of atherosclerotic carotid plaques: a study comparing acutely symptomatic and asymptomatic patients. Circ J 2010; 74: 2360-4.
25. Sadat U, Teng Z, Young VE, Graves MJ, Gaunt ME, Gillard JH. High-resolution magnetic resonance imaging-based biomechanical stress analysis of carotid atheroma: a comparison of single transient ischaemic attack, recurrent transient ischaemic attacks, non-disabling stroke and asymptomatic patient groups. Eur J Vasc Endovasc Surg 2011; 41: 83-90.
26. Sadat U, Teng Z, Young VE, Walsh SR, Li ZY, Graves MJ, et al. Association between biomechanical structural stresses of atherosclerotic carotid plaques and subsequent ischaemic cerebrovascular events - a longitudinal in vivo magnetic resonance imaging-based finite element study. Eur J Vasc Endovasc Surg 2010; 40: 485-91.
27. Teng Z, Brown AJ, Calvert PA, Parker RA, Obaid DR, Huang Y, et al. Coronary plaque structural stress is associated with plaque composition and subtype and higher in acute coronary syndrome: the BEACON I (Biomechanical Evaluation of Atheromatous Coronary Arteries) study. Circ Cardiovasc Imaging 2014; 7: 461-70.
28. Sadat U, Teng Z, Gillard JH. Biomechanical structural stresses of atherosclerotic plaques. Expert Rev Cardiovasc Ther 2010; 8: 1469-81.
29. Walsh MT, Cunnane EM, Mulvihill JJ, Akyildiz AC, Gijsen FJ, Holzapfel GA. Uniaxial tensile testing approaches for characterisation of atherosclerotic plaques. J Biomech 2014; 47: 793-804.
30. Learoyd BM, Taylor MG. Alterations with age in the viscoelastic properties of human arterial walls. Circ Res 1966; 18: 278-92.
31. Arbustini E, Morbini P, D'Armini AM, Repetto A, Minzioni G, Piovella F, et al. Plaque composition in plexogenic and thromboembolic pulmonary hypertension: the critical role of thrombotic material in pultaceous core formation. Heart 2002; 88: 177-82.
32. Teng Z, He J, Degnan AJ, Chen S, Sadat U, Bahaei NS, et al. Critical mechanical conditions around neovessels in carotid atherosclerotic plaque may promote intraplaque hemorrhage. Atherosclerosis 2012; 223: 321-6.
33. Kockx MM, Cromheeke KM, Knaapen MW, Bosmans JM, De Meyer GR, Herman AG, et al. Phagocytosis and macrophage activation associated with hemorrhagic microvessels in human atherosclerosis. Arterioscler Thromb Vasc Biol 2003; 23: 440-6.
34. Mackman N. Triggers, targets and treatments for thrombosis. Nature 2008; 451: 914-8.
35. Svindland A, Torvik A. Atherosclerotic carotid disease in asymptomatic individuals: an histological study of 53 cases. Acta Neurol Scand 1988; 78: 506-17.
36. Qiao Y, Farber A, Semaan E, Hamilton JA. Images in cardiovascular medicine. Healing of an asymptomatic carotid plaque ulceration. Circulation 2008; 118: e147-8.
37. Ebenstein DM, Coughlin D, Chapman J, Li C, Pruitt LA. Nanomechanical properties of calcification, fibrous tissue, and hematoma from atherosclerotic plaques. J Biomed Mater Res 2009; 91: 1028-37.
38. Teng Z, Tang D, Zheng J, Woodard PK, Hoffman AH. An experimental study on the ultimate strength of the adventitia and media of human atherosclerotic carotid arteries in circumferential and axial directions. J Biomech 2009; 42: 2535-9.
39. Maher E, Creane A, Sultan S, Hynes N, Lally C, Kelly DJ. Tensile and compressive properties of fresh human carotid atherosclerotic plaques. J Biomech 2009; 42: 2760-7.
40. Barrett SR, Sutcliffe MP, Howarth S, Li ZY, Gillard JH. Experimental measurement of the mechanical properties of carotid atherothrombotic plaque fibrous cap. J Biomech 2009; 42: 1650-5.
41. Lawlor MG, O'Donnell MR, O'Connell BM, Walsh MT. Experimental determination of circumferential properties of fresh carotid artery plaques. J Biomech 2011; 44: 1709-15.
42. Kural MH, Cai M, Tang D, Gwyther T, Zheng J, Billiar KL. Planar biaxial characterization of diseased human coronary and carotid arteries for computational modeling. J Biomech 2012; 45: 790-8.
43. Chai CK, Akyildiz AC, Speelman L, Gijsen FJ, Oomens CW, van Sambeek MR, et al. Local axial compressive mechanical properties of human carotid atherosclerotic plaques-characterisation by indentation test and inverse finite element analysis. J Biomech 2013; 46: 1759-66.
44. Mulvihill JJ, Cunnane EM, McHugh SM, Kavanagh EG, Walsh SR, Walsh MT. Mechanical, biological and structural characterization of in vitro ruptured human carotid plaque tissue. Acta Biomater 2013; 9: 9027-35.