A mechanistic analysis of the role of microcalcifications in atherosclerotic plaque stability: Potential implications for plaque rupture

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 303, Issue 5, 2012, Pages

  Maldonado, Natalia ^a   Kelly Arnold, Adreanne ^a   Vengrenyuk, Yuliya ^c   Laudier, Damien ^a   Fallon, John T ^d   Virmani, Renu ^e   Cardoso, Luis ^a   Weinbaum, Sheldon ^a,b  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c NEW YORK UNIVERSITY   (United States)

^d NEW YORK MEDICAL COLLEGE   (United States)

^e CVPATH INSTITUTE   (United States)

Author keywords

Coronary artery calcification; Coronary computed tomography; Finite element analysis; Vulnerable plaque

Indexed keywords

AGED; ARTERY CALCIFICATION; ARTICLE; ATHEROSCLEROTIC PLAQUE; BIOMECHANICS; CORONARY ARTERY; FEMALE; FINITE ELEMENT ANALYSIS; HISTOLOGY; HUMAN; HUMAN TISSUE; MALE; MICRO-COMPUTED TOMOGRAPHY; PRIORITY JOURNAL; YOUNG MODULUS;

AGED; BIOMECHANICS; COMPUTER SIMULATION; CORONARY ARTERY DISEASE; CORONARY VESSELS; ELASTIC MODULUS; FEMALE; FIBROSIS; FINITE ELEMENT ANALYSIS; HUMANS; IMAGING, THREE-DIMENSIONAL; MALE; MIDDLE AGED; MODELS, CARDIOVASCULAR; PLAQUE, ATHEROSCLEROTIC; RADIOGRAPHIC IMAGE INTERPRETATION, COMPUTER-ASSISTED; RUPTURE, SPONTANEOUS; STRESS, MECHANICAL; VASCULAR CALCIFICATION; X-RAY MICROTOMOGRAPHY;

EID: 84865749355     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00036.2012     Document Type: Article

References (47)

1. Aikawa E, Aikawa M, Libby P, Figueiredo JL, Rusanescu G, Iwamoto Y, Fukuda D, Kohler RH, Shi GP, Jaffer FA, Weissleder R. Arterial and aortic valve calcification abolished by elastolytic cathepsin S deficiency in chronic renal disease. Circulation 119: 1785-1794, 2009.
2. Aikawa E, Nahrendorf M, Figueiredo JL, Swirski FK, Shtatland T, Kohler RH, Jaffer FA, Aikawa M, Weissleder R. Osteogenesis associates with inflammation in early-stage atherosclerosis evaluated by molecular imaging in vivo. Circulation 116: 2841-2850, 2007.
3. Akyildiz AC, Speelman L, van Brummelen H, Gutiérrez MA, Virmani R, van der Lugt A, van der Steen AF, Wentzel JJ, Gijsen FJ. Effects of intima stiffness and plaque morphology on peak cap stress. Biomed Eng Online 10: 25, 2011.
4. Bluestein D, Alemu Y, Avrahami I, Gharib M, Dumont K, Ricotta JJ, Einav S. Influence of microcalcifications on vulnerable plaque mechanics using FSI modeling. J Biomech 41: 1111-1118, 2008.
5. Bobryshev YV, Killingsworth MC, Lord RS, Grabs AJ. Matrix vesicles in the fibrous cap of atherosclerotic plaque: possible contribution to plaque rupture. J Cell Mol Med 12: 2073-2082, 2008.
6. Burke AP, Kolodgie FD, Farb A, Virmani R. Pathogenesis and significance of calcification in coronary aterosclerosis. In: The Vulnerable Atherosclerotic Plaque: Strategies for Diagnosis and Management, edited by Virmani R, Narula J, Leon M, and Willerson JT. Malden, MA: Blackwell, 2007, p. 77-94.
7. Burke AP, Taylor A, Farb A, Malcom GT, Virmani R. Coronary calcification: insights from sudden coronary death victims. Z Kardiol 89, Suppl 2: 49-53, 2000.
8. Burke AP, Farb A, Malcom GT, Liang YH, Smialek J, Virmani R. Coronary risk factors and plaque morphology in men with coronary disease who died suddenly. N Engl J Med 336: 1276-1282, 1997.
9. Caro CG. Discovery of the role of wall shear in atherosclerosis. Arterioscler Thromb Vasc Biol 29: 158-161, 2009.
10. 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 87: 1179-1187, 1993.
11. Cheruvu PK, Finn AV, Gardner C, Caplan J, Goldstein J, Stone GW, Virmani R, Muller JE. Frequency and distribution of thin-cap fibroatheroma and ruptured plaques in human coronary arteries: a pathologic study. J Am Coll Cardiol 50: 940-949, 2007.
12. Ehara S, Kobayashi Y, Yoshiyama M, Shimada K, Shimada Y, Fukuda D, Nakamura Y, Yamashita H, Yamagishi H, Takeuchi K, Naruko T, Haze K, Becker AE, Yoshikawa J, Ueda M. Spotty calcification typifies the culprit plaque in patients with acute myocardial infarction: an intravascular ultrasound study. Circulation 110: 3424-3429, 2004.
13. Finet G, Ohayon J, Rioufol G. Biomechanical interaction between cap thickness, lipid core composition and blood pressure in vulnerable coronary plaque: impact on stability or instability. Coron Artery Dis 15: 13-20, 2004.
14. Fitzpatrick L, Severson A, Edwards WD, Ingram RT. Diffuse calcification in human coronary arteries. Association of osteopontin with atherosclerosis. J Clin Invest 94: 1597-1604, 1994.
15. Fujii K, Carlier SG, Mintz GS, Takebayashi H, Yasuda T, Costa RA, Moussa I, Dangas G, Mehran R, Lansky AJ, Kreps EM, Collins M, Stone GW, Moses JW, Leon MB. Intravascular ultrasound study of patterns of calcium in ruptured coronary plaques. Am J Cardiol 96: 352-357, 2005.
16. Gent AN. Detachment of an elastic matrix from a rigid spherical inclusion. J Mater Sci 15: 2884-2888, 1980.
17. Hoshino T, Chow LA, Hsu JJ, Perlowski AA, Abedin M, Tobis J, Tintut Y, Mal AK, Klug WS, Demer LL. Mechanical stress analysis of a rigid inclusion in distensible material: a model of atherosclerotic calcification and plaque vulnerability. Am J Physiol Heart Circ Physiol 297: H802-H810, 2009.
18. Huang H, Virmani R, Younis H, Burke AP, Kamm RD, Lee RT. The impact of calcification on the biomechanical stability of atherosclerotic plaques. Circulation 103: 1051-1056, 2001.
19. Kolodgie FD, Gold HK, Burke AP, Fowler DR, Kruth HS, Weber DK, Farb A, Guerrero LJ, Hayase M, Kutys R, Narula J, Finn AV, Virmani R. Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med 349: 2316-2325, 2003.
20. Kume T, Okura H, Kawamoto T, Yamada R, Miyamoto Y, Hayashida A, Watanabe N, Neishi Y, Sadahira Y, Akasaka T, Yoshida K. Assessment of the coronary calcification by optical coherence tomography. EuroIntervention 6: 768-772, 2011.
21. Langheinrich AC, Kampschulte M, Crössmann C, Moritz R, Rau WS, Bohle RM, Ritman EL. Role of computed tomography voxel size in detection and discrimination of calcium and iron deposits in atherosclerotic human coronary artery specimens. J Comput Assist Tomogr 33: 517-522, 2009.
22. Langheinrich AC, Michniewicz A, Sedding DG, Lai B, Jorgensen SM, Bohle RM, Ritman EL. Quantitative X-ray imaging of intraplaque hemorrhage in aortas of apoE(-/-)/LDL(-/-) double knockout mice. Invest Radiol 42: 263-273, 2007.
23. Laudier D, Schaffler M, Flatow E, Wang V. Novel procedure for high-fidelity tendon histology. J Orthop Res 25: 390-395, 2007.
24. Leach J, Rayz V, Soares B, Wintermark M, Mofrad M, Saloner D. Carotid atheroma rupture observed in vivo and FSI-predicted stress distribution based on pre-rupture imaging. Ann Biomed Eng 38: 2748-2765, 2010.
25. Li CY, Price C, Delisser K, Nasser P, Laudier D, Clement M, Jepsen KJ, Schaffler MB. Long-term disuse osteoporosis seems less sensitive to bisphosphonate treatment than other osteoporosis. J Bone Miner Res 20: 117-124, 2005.
26. Loree HM, Kamm RD, Stringfellow RG, Lee RT. Effects of fibrous cap thickness on peak circumferential stress in model atherosclerotic vessels. Circ Res 71: 850-858, 1992.
27. Maehara A, Mintz GS, Bui AB, Walter OR, Castagna MT, Canos D, Pichard AD, Satler LF, Waksman R, Suddath WO, Laird JR Jr, Kent KM, Weissman NJ. Morphologic and angiographic features of coronary plaque rupture detected by intravascular ultrasound. J Am Coll Cardiol 40: 904-910, 2002.
28. McCollough CH, Ulzheimer S, Halliburton SS, Shanneik K, White RD, Kalender WA. Coronary artery calcium: a multi-institutional, multimanufacturer international standard for quantification at cardiac CT. Radiology 243: 527-538, 2007.
29. New SE, Aikawa E. Molecular imaging insights into early inflammatory stages of arterial and aortic valve calcification. Circ Res 108: 1381-1391, 2011.
30. New SE, Aikawa E. Cardiovascular calcification: an inflammatory disease. Circ J 75: 1305-1313, 2011.
31. Ohayon J, Finet G, Treyve F, Rioufol G, Dubreuil O. A threedimensional finite element analysis of stress distribution in a coronary atherosclerotic plaque. Methods 661: 225-241, 2005.
32. Ohayon J, Dubreuil O, Tracqui P, Le Floc'h S, Rioufol G, Chalabreysse L, Thivolet F, Pettigrew RI, Finet G. Influence of residual stress/ strain on the biomechanical stability of vulnerable coronary plaques: potential impact for evaluating the risk of plaque rupture. Am J Physiol Heart Circ Physiol 293: H1987-H1996, 2007.
33. Ohayon J, Finet G, Gharib AM, Herzka DA, Tracqui P, Heroux J, Rioufol G, Kotys MS, Elagha A, Pettigrew RI. Necrotic core thickness and positive arterial remodeling index: emergent biomechanical factors for evaluating the risk of plaque rupture. Am J Physiol Heart Circ Physiol 295: H717-H727, 2008.
34. Rambhia SH, Liang X, Xenos M, Alemu Y, Maldonado N, Kelly A, Chakraborti S, Weinbaum S, Cardoso L, Einav S, Bluestein D. Microcalcifications increase coronary vulnerable plaque rupture potential: a patient-based micro-CT fluid-structure interaction study. Ann Biomed Eng 40: 1443-1454, 2012.
35. Relucenti M, Heyn R, Petruzziello L, Pugliese G, Taurino M, Familiari G. Detecting microcalcifications in atherosclerotic plaques by a simple trichromic staining method for epoxy embedded carotid endarterectomies. Eur J Histochem 54: e33, 2010.
36. Richardson P, Davies M, Born G. Influence of plaque configuration and stress distribution on fissuring of coronary atherosclerotic plaques. Lancet 2: 941-944, 1989.
37. Roijers R, Debernardi N, Cleutjens J, Schurgers L, Mutsaers P, van der Vusse G. Microcalcifications in early intimal lesions of atherosclerotic human coronary arteries. Am J Pathol 178: 2879-2887, 2011.
38. Sangiorgi G, Rumberger JA, Severson A, Edwards WD, Gregoire J, Fitzpatrick LA, Schwartz RS. Arterial calcification and not lumen stenosis is highly correlated with atherosclerotic plaque burden in humans: a histologic study of 723 coronary artery segments using nondecalcifying methodology. J Am Coll Cardiol 31: 126-133, 1998.
39. Tanaka A, Imanishi T, Kitabata H, Kubo T, Takarada S, Tanimoto T, Kuroi A, Tsujioka H, Ikejima H, Ueno S, Kataiwa H, Okouchi K, Kashiwaghi M, Matsumoto H, Takemoto K, Nakamura N, Hirata K, Mizukoshi M, Akasaka T. Morphology of exertion-triggered plaque rupture in patients with acute coronary syndrome: an optical coherence tomography study. Circulation 118: 2368-2373, 2008.
40. Tang D, Yang C, Zheng J, Woodard PK, Saffitz JE, Petruccelli JD, Sicard GA, Yuan C. Local maximal stress hypothesis and computational plaque vulnerability index for atherosclerotic plaque assessment. Ann Biomed Eng 33: 1789-1801, 2005.
41. Teng Z, Canton G, Yuan C, Ferguson M, Yang C, Huang X, Zheng J, Woodard PK, Tang D. 3D critical plaque wall stress is a better predictor of carotid plaque rupture sites than flow shear stress: an in vivo MRI-based 3D FSI study. J Biomech Eng 132: 031007, 2010.
42. Thilo C, Gebregziabher M, Mayer F, Schoepf J. Correlation of regional distribution and morphological pattern of calcification. Eur Radiol 20: 855-861, 2010.
43. Vengrenyuk Y, Cardoso L, Weinbaum S. Micro CT based analysis of a new paradigm for vulnerable plaque rupture: cellular microcalcifications in fibrous caps. Mol Cell Biomech 5: 37-47, 2008.
44. Vengrenyuk Y, Weinbaum S, Carlier S, Xanthos S, Cardoso L, Ganatos P, Virmani R, Einav S, Gilchrist L. A hypothesis for vulnerable plaque rupture due to stress-induced debonding around cellular microcalcifications in thin fibrous caps. Proc Natl Acad Sci USA 103: 14678-14683, 2006.
45. Virmani R, Burke AP, Kolodgie FD, Farb A. Pathology of the thin-cap fibroatheroma: a type of vulnerable plaque. J Interv Cardiol 16: 267-272, 2003.
46. Virmani R, Narula J, Leon M, Willerson JT. (Editors). The Vulnerable Atherosclerotic Plaque: Strategies for Diagnosis and Management. Malden, MA: Blackwell, 2007.
47. Wenk JF, Papadopoulos P, Zohdi TI. Numerical modeling of stress in stenotic arteries with microcalcifications: a micromechanical approximation. J Biomech Eng 132: 091011, 2010.