Coronary artery wall shear stress is associated with progression and transformation of atherosclerotic plaque and arterial remodeling in patients with coronary artery disease

Circulation

Volumn 124, Issue 7, 2011, Pages 779-788

  Samady, Habib ^a   Eshtehardi, Parham ^a   McDaniel, Michael C ^a   Suo, Jin ^b   Dhawan, Saurabh S ^a   Maynard, Charles ^c   Timmins, Lucas H ^a,b   Quyyumi, Arshed A ^a   Giddens, Don P ^b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

atherosclerosis; coronary artery disease; hemodynamics; interventional; intravascular ultrasonography; wall shear stress

Indexed keywords

ADULT; AGED; ARTERY WALL; ARTICLE; ATHEROSCLEROTIC PLAQUE; BLOOD VESSEL CALCIFICATION; BLOOD VESSEL DIAMETER; CLINICAL ARTICLE; COMPUTATIONAL FLUID DYNAMICS; CORONARY ARTERY DISEASE; DISEASE ASSOCIATION; DISEASE COURSE; FEMALE; HUMAN; INTRAVASCULAR ULTRASOUND; MALE; PRIORITY JOURNAL; SHEAR STRESS; VASCULAR NECROSIS;

AGED; CALCINOSIS; CORONARY ARTERY DISEASE; CORONARY VESSELS; DISEASE PROGRESSION; FEMALE; FIBROSIS; HUMANS; HYDRODYNAMICS; MALE; MIDDLE AGED; NECROSIS; PLAQUE, ATHEROSCLEROTIC; PROSPECTIVE STUDIES; STRESS, MECHANICAL; ULTRASONOGRAPHY, INTERVENTIONAL;

EID: 80051949293     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.111.021824     Document Type: Article

References (63)

1. Davies PF. Flow-mediated endothelial mechanotransduction. Physiol Rev. 1995;75:519-560.
2. Dhawan SS, Avati Nanjundappa RP, Branch JR, Taylor WR, Quyyumi AA, Jo H, McDaniel MC, Suo J, Giddens D, Samady H. Shear stress and plaque development. Expert Rev Cardiovasc Ther. 2010;8:545-556.
3. Koskinas KC, Chatzizisis YS, Baker AB, Edelman ER, Stone PH, Feldman CL. The role of low endothelial shear stress in the conversion of atherosclerotic lesions from stable to unstable plaque. Curr Opin Cardiol. 2009;24:580-590.
4. Giddens DP, Zarins CK, Glagov S. The role of fluid mechanics in the localization and detection of atherosclerosis. J Biomech Eng. 1993;115: 588-594. (Pubitemid 24000887)
5. Glagov S, Bassiouny HS, Giddens DP, Zarins CK. Pathobiology of plaque modeling and complication. Surg Clin North Am. 1995;75: 545-556.
6. Koskinas KC, Feldman CL, Chatzizisis YS, Coskun AU, Jonas M, Maynard C, Baker AB, Papafaklis MI, Edelman ER, Stone PH. Natural history of experimental coronary atherosclerosis and vascular remodeling in relation to endothelial shear stress: a serial, in vivo intravascular ultrasound study. Circulation. 2010;121:2092-2101.
7. Cheng C, Tempel D, van Haperen R, Van Der Baan A, Grosveld F, Daemen MJ, Krams R, de Crom R. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation. 2006;113:2744-2753. (Pubitemid 43947992)
8. Nam D, Ni C, Rezvan A, Suo J, Budzyn K, Llanos A, Harrison D, Giddens D, Jo H. Partial carotid ligation is a model of acutely induced disturbed flow, leading to rapid endothelial dysfunction and atherosclerosis. Am J Physiol Heart Circ Physiol. 2009;297:H1535-H1543.
9. Zarins CK, Giddens DP, Bharadvaj BK, Sottiurai VS, Mabon RF, Glagov S. Carotid bifurcation atherosclerosis: quantitative correlation of plaque localization with flow velocity profiles and wall shear stress. Circ Res. 1983;53:502-514. (Pubitemid 14231103)
10. Stone PH, Coskun AU, Kinlay S, Popma JJ, Sonka M, Wahle A, Yeghiazarians Y, Maynard C, Kuntz RE, Feldman CL. Regions of low endothelial shear stress are the sites where coronary plaque progresses and vascular remodelling occurs in humans: an in vivo serial study. Eur Heart J. 2007;28:705-710. (Pubitemid 46439242)
11. Kenagy RD, Fischer JW, Davies MG, Berceli SA, Hawkins SM, Wight TN, Clowes AW. Increased plasmin and serine proteinase activity during flow-induced intimal atrophy in baboon PTFE grafts. Arterioscler Thromb Vasc Biol. 2002;22:400-404. (Pubitemid 34218745)
12. Lijnen HR. Plasmin and matrix metalloproteinases in vascular remodeling. Thromb Haemost. 2001;86:324-333. (Pubitemid 32663963)
13. Chatzizisis YS, Baker AB, Sukhova GK, Koskinas KC, Papafaklis MI, Beigel R, Jonas M, Coskun AU, Stone BV, Maynard C, Shi GP, Libby P, Feldman CL, Edelman ER, Stone PH. Augmented expression and activity of extracellular matrix-degrading enzymes in regions of low endothelial shear stress colocalize with coronary atheromata with thin fibrous caps in pigs. Circulation. 2011;123:621-630.
14. Casey PJ, Dattilo JB, Dai G, Albert JA, Tsukurov OI, Orkin RW, Gertler JP, Abbott WM. The effect of combined arterial hemodynamics on saphenous venous endothelial nitric oxide production. J Vasc Surg. 2001; 33:1199-1205.
15. Kolpakov V, Gordon D, Kulik TJ. Nitric oxide-generating compounds inhibit total protein and collagen synthesis in cultured vascular smooth muscle cells. Circ Res. 1995;76:305-309.
16. Mintz GS, Nissen SE, Anderson WD, Bailey SR, Erbel R, Fitzgerald PJ, Pinto FJ, Rosenfield K, Siegel RJ, Tuzcu EM, Yock PG. American college of cardiology clinical expert consensus document on standards for acquisition, measurement and reporting of intravascular ultrasound studies (IVUS): a report of the American College of Cardiology Task Force on Clinical Expert Consensus Documents. J Am Coll Cardiol. 2001;37:1478-1492.
17. Nair A, Margolis MP, Kuban BD, Vince DG. Automated coronary plaque characterisation with intravascular ultrasound backscatter: ex vivo validation. EuroIntervention. 2007;3:113-120.
18. 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. 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. 2006;47:2405-2412. (Pubitemid 43866370)
19. Garcia-Garcia H, Mintz G, Lerman A, Vince G, Margolis P, van ESG, Morel MA, Nair A, Virmani R, Burke A, Stone G, Serruys PW. Tissue characterisation using intravascular radiofrequency data analysis: recommendations for acquisition, analysis, interpretation and reporting. EuroIntervention. 2009;5:177-189.
20. Mintz GS, Garcia-Garcia HM, Nicholls SJ, Weissman NJ, Bruining N, Crowe T, Tardif J-C, Serruys PW. Clinical expert consensus document on standards for acquisition, measurement and reporting of intravascular ultrasound regression/progression studies. EuroIntervention. 2011;6: 1123-1130.
21. Sipahi I, Tuzcu EM, Schoenhagen P, Nicholls SJ, Crowe T, Kapadia S, Nissen SE. Static and serial assessments of coronary arterial remodeling are discordant: an intravascular ultrasound analysis from the Reversal of Atherosclerosis With Aggressive Lipid Lowering (REVERSAL) trial. Am Heart J. 2006;152:544-550. (Pubitemid 44233422)
22. Ku DN. Blood flow in arteries. Annu Rev Fluid Mech. 1997;29:399-434.
23. Jin S, Oshinski J, Giddens DP. Effects of wall motion and compliance on flow patterns in the ascending aorta. J Biomech Eng. 2003;125:347-354. (Pubitemid 36876428)
24. Suo J, Oshinski JN, Giddens DP. Blood flow patterns in the proximal human coronary arteries: relationship to atherosclerotic plaque occurrence. Mol Cell Biomech. 2008;5:9-18. (Pubitemid 351791113)
25. Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA. 1999;282:2035-2042.
26. Gimbrone MA Jr, Topper JN, Nagel T, Anderson KR, Garcia-Cardena G. Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann N Y Acad Sci. 2000;902:230-239.
27. Lin LI. A concordance correlation coefficient to evaluate reproducibility. Biometrics. 1989;45:255-268.
28. Barakat AI, Davies PF. Mechanisms of shear stress transmission and transduction in endothelial cells. Chest. 1998;114(suppl):58S-63S. (Pubitemid 28334865)
29. Suo J, Ferrara DE, Sorescu D, Guldberg RE, Taylor WR, Giddens DP. Hemodynamic shear stresses in mouse aortas: implications for atherogenesis. Arterioscler Thromb Vasc Biol. 2007;27:346-351. (Pubitemid 46143050)
30. Chatzizisis YS, Jonas M, Coskun AU, Beigel R, Stone BV, Maynard C, Gerrity RG, Daley W, Rogers C, Edelman ER, Feldman CL, Stone PH. Prediction of the localization of high-risk coronary atherosclerotic plaques on the basis of low endothelial shear stress: an intravascular ultrasound and histopathology natural history study. Circulation. 2008; 117:993-1002.
31. Stone PH, Coskun AU, Kinlay S, Clark ME, Sonka M, Wahle A, Ilegbusi OJ, Yeghiazarians Y, Popma JJ, Orav J, Kuntz RE, Feldman CL. Effect of endothelial shear stress on the progression of coronary artery disease, vascular remodeling, and in-stent restenosis in humans: in vivo 6-month follow-up study. Circulation. 2003;108:438-444. (Pubitemid 36935537)
32. Buchanan JR Jr, Kleinstreuer C, Truskey GA, Lei M. Relation between non-uniform hemodynamics and sites of altered permeability and lesion growth at the rabbit aorto-celiac junction. Atherosclerosis. 1999;143: 27-40. (Pubitemid 29138701)
33. Traub O, Berk BC. Laminar shear stress: mechanisms by which endothelial cells transduce an atheroprotective force. Arterioscler Thromb Vasc Biol. 1998;18:677-685. (Pubitemid 28267645)
34. Himburg HA, Grzybowski DM, Hazel AL, LaMack JA, Li XM, Friedman MH. Spatial comparison between wall shear stress measures and porcine arterial endothelial permeability. Am J Physiol Heart Circ Physiol. 2004; 286:H1916-H1922. (Pubitemid 38525482)
35. Chatzizisis YS, Coskun AU, Jonas M, Edelman ER, Feldman CL, Stone PH. Role of endothelial shear stress in the natural history of coronary atherosclerosis and vascular remodeling: molecular, cellular, and vascular behavior. J Am Coll Cardiol. 2007;49:2379-2393. (Pubitemid 46962266)
36. Goldstein JL, Kita T, Brown MS. Defective lipoprotein receptors and atherosclerosis: lessons from an animal counterpart of familial hypercholesterolemia. N Engl J Med. 1983;309:288-296. (Pubitemid 13074920)
37. Feldman CL, Ilegbusi OJ, Hu Z, Nesto R, Waxman S, Stone PH. Determination of in vivo velocity and endothelial shear stress patterns with phasic flow in human coronary arteries: a methodology to predict progression of coronary atherosclerosis. Am Heart J. 2002;143:931-939. (Pubitemid 34666876)
38. Bentzon JF, Weile C, Sondergaard CS, Hindkjaer J, Kassem M, Falk E. Smooth muscle cells in atherosclerosis originate from the local vessel wall and not circulating progenitor cells in ApoE knockout mice. Arterioscler Thromb Vasc Biol. 2006;26:2696-2702.
39. Ziegler T, Bouzourene K, Harrison VJ, Brunner HR, Hayoz D. Influence of oscillatory and unidirectional flow environments on the expression of endothelin and nitric oxide synthase in cultured endothelial cells. Arterioscler Thromb Vasc Biol. 1998;18:686-692. (Pubitemid 28267646)
40. Conklin BS, Zhong DS, Zhao W, Lin PH, Chen C. Shear stress regulates occludin and VEGF expression in porcine arterial endothelial cells. J Surg Res. 2002;102:13-21.
41. Nissen SE, Nicholls SJ, Sipahi I, Libby P, Raichlen JS, Ballantyne CM, Davignon J, Erbel R, Fruchart JC, Tardif JC, Schoenhagen P, Crowe T, Cain V, Wolski K, Goormastic M, Tuzcu EM. Effect of very highintensity statin therapy on regression of coronary atherosclerosis: the ASTEROID trial. JAMA. 2006;295:1556-1565.
42. Nissen SE, Tuzcu EM, Schoenhagen P, Brown BG, Ganz P, Vogel RA, Crowe T, Howard G, Cooper CJ, Brodie B, Grines CL, DeMaria AN. Effect of intensive compared with moderate lipid-lowering therapy on progression of coronary atherosclerosis: a randomized controlled trial. JAMA. 2004;291:1071-1080. (Pubitemid 38541684)
43. Hong MK, Park DW, Lee CW, Lee SW, Kim YH, Kang DH, Song JK, Kim JJ, Park SW, Park SJ. Effects of statin treatments on coronary plaques assessed by volumetric virtual histology intravascular ultrasound analysis. JACC Cardiovasc Interv. 2009;2:679-688.
44. Nasu K, Tsuchikane E, Katoh O, Tanaka N, Kimura M, Ehara M, Kinoshita Y, Matsubara T, Matsuo H, Asakura K, Asakura Y, Terashima M, Takayama T, Honye J, Hirayama A, Saito S, Suzuki T. Effect of fluvastatin on progression of coronary atherosclerotic plaque evaluated by virtual histology intravascular ultrasound. JACC Cardiovasc Interv. 2009; 2:689-696.
45. Samady H, McDaniel MC. Can statins alter coronary plaque composition assessed by radiofrequency backscatter intravascular ultrasound? JACC Cardiovasc Interv. 2009;2:697-700.
46. Cannon CP, Braunwald E, McCabe CH, Rader DJ, Rouleau JL, Belder R, Joyal SV, Hill KA, Pfeffer MA, Skene AM. Intensive versus moderate lipid lowering with statins after acute coronary syndromes. N Engl J Med. 2004;350:1495-1504. (Pubitemid 38477774)
47. Finn AV, Nakano M, Narula J, Kolodgie FD, Virmani R. Concept of vulnerable/unstable plaque. Arterioscler Thromb Vasc Biol. 2010;30: 1282-1292.
48. Stone GW, Maehara A, Lansky AJ, de Bruyne B, Cristea E, Mintz GS, Mehran R, McPherson J, Farhat N, Marso SP, Parise H, Templin B, White R, Zhang Z, Serruys PW. A prospective natural-history study of coronary atherosclerosis. N Engl J Med. 2011;364:226-235.
49. Fukumoto Y, Hiro T, Fujii T, Hashimoto G, Fujimura T, Yamada J, Okamura T, Matsuzaki M. Localized elevation of shear stress is related to coronary plaque rupture: a 3-dimensional intravascular ultrasound study with in-vivo color mapping of shear stress distribution. J Am Coll Cardiol. 2008;51:645-650. (Pubitemid 351193102)
50. Gijsen FJH, Wentzel JJ, Thury A, Mastik F, Schaar JA, Schuurbiers JCH, Slager CJ, Van Der Giessen WJ, de Feyter PJ, Van Der Steen AFW, Serruys PW. Strain distribution over plaques in human coronary arteries relates to shear stress. Am J Physiol Heart Circ Physiol. 2008;295:H1608-H1614.
51. Groen H, Gijsen F, Van Der Lugt A, Ferguson M, Hatsukami T, Van Der Steen A, Yuan C, Wentzel J. Plaque rupture in the carotid artery is localized at the high shear stress region: a case report. Stroke. 2007;38: 2379-2381. (Pubitemid 47457588)
52. Tang D, Teng Z, Canton G, Yang C, Ferguson M, Huang X, Zheng J, Woodard P, Yuan C. Sites of rupture in human atherosclerotic carotid plaques are associated with high structural stresses: an in vivo MRI-based 3D fluid-structure interaction study. Stroke. 2009;40:3258-3263.
53. Dirksen MT, Van Der Wal AC, van den Berg FM, Van Der Loos CM, Becker AE. Distribution of inflammatory cells in atherosclerotic plaques relates to the direction of flow. Circulation. 1998;98:2000-2003. (Pubitemid 28512223)
54. Naghavi M, Libby P, Falk E, Casscells SW, Litovsky S, Rumberger J, Badimon JJ, Stefanadis C, Moreno P, Pasterkamp G, Fayad Z, Stone PH, Waxman S, Raggi P, Madjid M, Zarrabi A, Burke A, Yuan C, Fitzgerald PJ, Siscovick DS, de Korte CL, Aikawa M, Juhani Airaksinen KE, Assmann G, Becker CR, Chesebro JH, Farb A, Galis ZS, Jackson C, Jang IK, Koenig W, Lodder RA, March K, Demirovic J, Navab M, Priori SG, Rekhter MD, Bahr R, Grundy SM, Mehran R, Colombo A, Boerwinkle E, Ballantyne C, Insull W Jr, Schwartz RS, Vogel R, Serruys PW, Hansson GK, Faxon DP, Kaul S, Drexler H, Greenland P, Muller JE, Virmani R, Ridker PM, Zipes DP, Shah PK, Willerson JT. From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: part I. Circulation. 2003;108:1664-1672. (Pubitemid 37243650)
55. Slager CJ, Wentzel JJ, Gijsen FJ, Schuurbiers JC, Van Der Wal AC, Van Der Steen AF, Serruys PW. The role of shear stress in the generation of rupture-prone vulnerable plaques. Nat Clin Pract Cardiovasc Med. 2005; 2:401-407. (Pubitemid 41094126)
56. Mattsson EJR, Kohler TR, Vergel SM, Clowes AW. Increased blood flow induces regression of intimal hyperplasia. Arterioscler Thromb Vasc Biol. 1997;17:2245-2249. (Pubitemid 28057128)
57. Death AK, Nakhla S, McGrath KC, Martell S, Yue DK, Jessup W, Celermajer DS. Nitroglycerin upregulates matrix metalloproteinase expression by human macrophages. J Am Coll Cardiol. 2002;39: 1943-1950. (Pubitemid 34628274)
58. Bark DL Jr, Ku DN. Wall shear over high degree stenoses pertinent to atherothrombosis. J Biomech. 2010;43:2970-2977.
59. Ibrahim J, Miyashiro JK, Berk BC. Shear stress is differentially regulated among inbred rat strains. Circ Res. 2003;92:1001-1009. (Pubitemid 36588499)
60. Korshunov VA, Berk BC. Strain-dependent vascular remodeling: the "Glagov phenomenon" is genetically determined. Circulation. 2004;110: 220-226. (Pubitemid 38924591)
61. Thim T, Hagensen MK, Wallace-Bradley D, Granada JF, Kaluza GL, Drouet L, Paaske WP, Botker HE, Falk E. Unreliable assessment of necrotic core by virtual histology intravascular ultrasound in porcine coronary artery disease. Circ Cardiovasc Imaging. 2010;3:384-391.
62. Nair A, Kuban BD, Tuzcu EM, Schoenhagen P, Nissen SE, Vince DG. Coronary plaque classification with intravascular ultrasound radiofrequency data analysis. Circulation. 2002;106:2200-2206. (Pubitemid 35222213)
63. Third report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) final report. Circulation. 2002; 106:3143-3421.