Vascular inflammation and repair: Implications for re-endothelialization, restenosis, and stent thrombosis

JACC: Cardiovascular Interventions

Volumn 4, Issue 10, 2011, Pages 1057-1066

  Inoue, Teruo ^a   Croce, Kevin ^b,c   Morooka, Toshifumi ^d   Sakuma, Masashi ^e   Node, Koichi ^e   Simon, Daniel I ^d  

^a DOKKYO MEDICAL UNIVERSITY   (Japan)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Veteran's Administration Healthcare System   (United States)

^d UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^e SAGA UNIVERSITY   (Japan)

Author keywords

inflammation; re endothelialization; restenosis; stent thrombosis

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; ANTITHROMBOCYTIC AGENT; CYTOKINE; EVEROLIMUS; GRANULOCYTE COLONY STIMULATING FACTOR; PACLITAXEL; PHOSPHATIDYLINOSITOL 3 KINASE; RAPAMYCIN; STROMAL CELL DERIVED FACTOR 1; ZOTAROLIMUS;

APOPTOSIS; ARTERY INTIMA PROLIFERATION; ARTICLE; BARE METAL STENT; BLOOD VESSEL; BONE MARROW; CONTINUING EDUCATION; CORONARY ARTERY DISEASE; CORONARY STENT; DIABETES MELLITUS; DRUG ELUTING STENT; ENZYME ACTIVITY; HUMAN; IMMUNE SYSTEM; IN-STENT RESTENOSIS; INFLAMMATION; PERCUTANEOUS CORONARY INTERVENTION; PRIORITY JOURNAL; STEM CELL; STENT THROMBOSIS; THROMBOSIS; TISSUE REPAIR; VASCULAR ENDOTHELIUM;

EID: 80054993002     PISSN: 19368798     EISSN: 18767605     Source Type: Journal    
DOI: 10.1016/j.jcin.2011.05.025     Document Type: Review

References (90)

1. Y. Gouffic, S. Potter-Perigo, and C.K. Chan Sirolimus blocks the accumulation of hyaluronan (HA) by arterial smooth muscle cells and reduces monocyte adhesion to the ECM Atherosclerosis 195 2007 23 30 (Pubitemid 47561940)
2. M. Hilker, M. Buerke, and M. Guckenbiehl Rapamycin reduces neointima formation during vascular injury VASA 32 2003 10 13 (Pubitemid 36286273)
3. J. Park, H. Ha, and H.J. Ahn Sirolimus inhibits platelet-derived growth factor-induced collagen synthesis in rat vascular smooth muscle cells Transplant Proc 37 2005 3459 3462 (Pubitemid 41659921)
4. V. Bhatia, R. Bhatia, and M. Dhindsa Drug-eluting stents: new era and new concerns Postgrad Med J 80 2004 13 18 (Pubitemid 38221875)
5. M.A. Costa, and D.I. Simon Molecular basis of restenosis and drug-eluting stents Circulation 111 2005 2257 2273 (Pubitemid 40632443)
6. P.A. Lemos, C.A. van Mieghem, and C.A. Arampatzis Post-sirolimus-eluting stent restenosis treated with repeat percutaneous intervention: late angiographic and clinical outcomes Circulation 109 2004 2500 2502 (Pubitemid 38720546)
7. P. Garg, and L. Mauri The conundrum of late and very late stent thrombosis following drug-eluting stent implantation Curr Opin Cardiol 22 2007 565 571 (Pubitemid 47537941)
8. E.P. McFadden, E. Stabile, and E. Regar Late thrombosis in drug-eluting coronary stents after discontinuation of antiplatelet therapy Lancet 364 2004 1519 1521 (Pubitemid 39410418)
9. M.W. Webster, and J.A. Ormiston Drug-eluting stents and late stent thrombosis Lancet 370 2007 914 915 (Pubitemid 47384835)
10. R. Jaffe, and B.H. Strauss Late and very late thrombosis of drug-eluting stents: evolving concepts and perspectives J Am Coll Cardiol 50 2007 119 127 (Pubitemid 47007738)
11. M. Joner, A.V. Finn, and A. Farb Pathology of drug-eluting stents in humans: delayed healing and late thrombotic risk J Am Coll Cardiol 48 2006 193 202 (Pubitemid 43929240)
12. G. Nakazawa, A.V. Finn, and M. Joner Delayed arterial healing and increased late stent thrombosis at culprit sites after drug-eluting stent placement for acute myocardial infarction patients: an autopsy study Circulation 118 2008 1138 1145
13. J. Kotani, M. Awata, and S. Nanto Incomplete neointimal coverage of sirolimus-eluting stents: angioscopic findings J Am Coll Cardiol 47 2006 2108 2111
14. A.V. Finn, M. Joner, and G. Nakazawa Pathological correlates of late drug-eluting stent thrombosis: strut coverage as a marker of endothelialization Circulation 115 2007 2435 2441 (Pubitemid 46717966)
15. A.V. Finn, G. Nakazawa, and M. Joner Vascular responses to drug eluting stents: importance of delayed healing Arterioscler Thromb Vasc Biol 27 2007 1500 1510 (Pubitemid 46986103)
16. K. Croce, and P. Libby Intertwining of thrombosis and inflammation in atherosclerosis Curr Opin Hematol 14 2007 55 61 (Pubitemid 44885613)
17. A.V. Finn, F.D. Kolodgie, and J. Harnek Differential response of delayed healing and persistent inflammation at sites of overlapping sirolimus- or paclitaxel-eluting stents Circulation 112 2005 270 278 (Pubitemid 40982311)
18. J.R. Nebeker, R. Virmani, and C.L. Bennett Hypersensitivity cases associated with drug-eluting coronary stents: a review of available cases from the Research on Adverse Drug events And Reports (RADAR) project J Am Coll Cardiol 47 2006 175 181 (Pubitemid 43005183)
19. R. Virmani, G. Guagliumi, and A. Farb Localized hypersensitivity and late coronary thrombosis secondary to a sirolimus-eluting stent: should we be cautious? Circulation 109 2004 701 705 (Pubitemid 38222887)
20. M.A. Pallero, M. Talbert Roden, and Y.F. Chen Stainless steel ions stimulate increased thrombospondin-1-dependent TGF-beta activation by vascular smooth muscle cells: implications for in-stent restenosis J Vasc Res 47 2010 309 322
21. R.A. Byrne, M. Joner, and A. Kastrati Polymer coatings and delayed arterial healing following drug-eluting stent implantation Minerva Cardioangiol 57 2009 567 584
22. G.J. Wilson, G. Nakazawa, and R.S. Schwartz Comparison of inflammatory response after implantation of sirolimus- and paclitaxel-eluting stents in porcine coronary arteries Circulation 120 2009 141 149 12
23. S. Fuke, K. Maekawa, and K. Kawamoto Impaired endothelial vasomotor function after sirolimus-eluting stent implantation Circ J 71 2007 220 225 (Pubitemid 46182696)
24. D.I. Shin, P.J. Kim, and K.B. Seung Drug-eluting stent implantation could be associated with long-term coronary endothelial dysfunction Int Heart J 48 2007 553 567
25. K. Maekawa, K. Kawamoto, and S. Fuke Images in cardiovascular medicine Severe endothelial dysfunction after sirolimus-eluting stent implantation Circulation 113 2006 e850 e851 (Pubitemid 43943437)
26. M. Togni, S. Windecker, and R. Cocchia Sirolimus-eluting stents associated with paradoxic coronary vasoconstriction J Am Coll Cardiol 46 2005 231 236 (Pubitemid 40966848)
27. S.H. Hofma, W.J. van der Giessen, and B.M. van Dalen Indication of long-term endothelial dysfunction after sirolimus-eluting stent implantation Eur Heart J 27 2006 166 170 (Pubitemid 43069032)
28. B. Tesfamariam Drug release kinetics from stent device-based delivery systems J Cardiovasc Pharmacol 51 2008 118 125 (Pubitemid 351301471)
29. K.R. Kamath, J.J. Barry, and K.M. Miller The Taxus drug-eluting stent: a new paradigm in controlled drug delivery Adv Drug Deliv Rev 58 2006 412 436 (Pubitemid 43949060)
30. J. Waugh, and A.J. Wagstaff The paclitaxel (TAXUS)-eluting stent: a review of its use in the management of de novo coronary artery lesions Am J Cardiovasc Drugs 4 2004 257 268 (Pubitemid 39206620)
31. K. McKeage, D. Murdoch, and K.L. Goa The sirolimus-eluting stent: a review of its use in the treatment of coronary artery disease Am J Cardiovasc Drugs 3 2003 211 230 (Pubitemid 36849568)
32. V.K. Raman, and E.R. Edelman Coated stents: local pharmacology Semin Interv Cardiol 3 1998 133 137
33. D.I. Shin, K.B. Seung, and P.J. Kim Long-term coronary endothelial function after zotarolimus-eluting stent implantation A 9 month comparison between zotarolimus-eluting and sirolimus-eluting stents Int Heart J 49 2008 639 652
34. J.W. Kim, S.Y. Suh, and C.U. Choi Six-month comparison of coronary endothelial dysfunction associated with sirolimus-eluting stent versus paclitaxel-eluting stent J Am Coll Cardiol Intv 1 2008 65 71 (Pubitemid 351445416)
35. M.I. Hamilos, M. Ostojic, and B. Beleslin Differential effects of drug-eluting stents on local endothelium-dependent coronary vasomotion J Am Coll Cardiol 51 2008 2123 2129 (Pubitemid 351721001)
36. P. Thanyasiri, K. Kathir, D.S. Celermajer, and M.R. Adams Endothelial dysfunction and restenosis following percutaneous coronary intervention Int J Cardiol 119 2007 362 367 (Pubitemid 46921269)
37. A.A. Bavry, D.J. Kumbhani, T.J. Helton, and D.L. Bhatt Risk of thrombosis with the use of sirolimus-eluting stents for percutaneous coronary intervention (from registry and clinical trial data) Am J Cardiol 95 2005 1469 1472 (Pubitemid 40824771)
38. A.A. Bavry, D.J. Kumbhani, T.J. Helton, and D.L. Bhatt What is the risk of stent thrombosis associated with the use of paclitaxel-eluting stents for percutaneous coronary intervention?: A meta-analysis J Am Coll Cardiol 45 2005 941 946 (Pubitemid 40342823)
39. D.E. Cutlip, S. Windecker, and R. Mehran Clinical end points in coronary stent trials: a case for standardized definitions Circulation 115 2007 2344 2351 (Pubitemid 46685903)
40. R. Moreno, C. Fernández, and R. Hernández Drug-eluting stent thrombosis: results from a pooled analysis including 10 randomized studies J Am Coll Cardiol 45 2005 954 959 (Pubitemid 40342825)
41. C. Stettler, S. Wandel, and S. Allemann Outcomes associated with drug-eluting and bare-metal stents: a collaborative network meta-analysis Lancet 370 2007 937 948 (Pubitemid 47393576)
42. A.T. Ong, A. Hoye, and J. Aoki Thirty-day incidence and six-month clinical outcome of thrombotic stent occlusion after bare-metal, sirolimus, or paclitaxel stent implantation J Am Coll Cardiol 45 2005 947 953 (Pubitemid 40342824)
43. A.T. Ong, P.W. Serruys, and J. Aoki The unrestricted use of paclitaxel-versus sirolimus-eluting stents for coronary artery disease in an unselected population: one-year results of the Taxus-Stent Evaluated at Rotterdam Cardiology Hospital (T-SEARCH) registry J Am Coll Cardiol 45 2005 1135 1141 (Pubitemid 40432449)
44. P. Urban, A.H. Gershlick, and G. Guagliumi Safety of coronary sirolimus-eluting stents in daily clinical practice: one-year follow-up of the e-Cypher registry Circulation 113 2006 1434 1441 (Pubitemid 43739440)
45. D.O. Williams, J.D. Abbott, K.E. Kip DEScover Investigators Outcomes of 6906 patients undergoing percutaneous coronary intervention in the era of drug-eluting stents: report of the DEScover Registry Circulation 114 2006 2154 2162 (Pubitemid 44747896)
46. H. Tanaka, G.K. Sukhova, and S.J. Swanson Sustained activation of vascular cells and leukocytes in the rabbit aorta after balloon injury Circulation 88 1993 1788 1803 (Pubitemid 23296926)
47. F.G. Welt, and C. Rogers Inflammation and restenosis in the stent era Arterioscler Thromb Vasc Biol 22 2002 1769 1776 (Pubitemid 35315761)
48. F.G. Welt, E.R. Edelman, D.I. Simon, and C. Rogers Neutrophil, not macrophage, infiltration precedes neointimal thickening in balloon-injured arteries Arterioscler Thromb Vasc Biol 20 2000 2553 2558
49. V. Evangelista, S. Manarini, and S. Rontondo Platelet/polymorphonuclear leukocyte interaction in dynamic conditions: evidence of adhesion cascade and cross talk between P-selectin and the b2 integrin cd11b/cd18 Blood 88 1996 4183 4194 (Pubitemid 26399164)
50. S.A. Hamburger, and R.P. McEver Gmp-140 mediates adhesion of stimulated platelets to neutrophils Blood 75 1990 550 554 (Pubitemid 20069190)
51. E. Larsen, A. Celi, and G.E. Gilbert PADGEM protein: a receptor that mediates the interaction of activated platelets with neutrophils and monocytes Cell 59 1989 305 312 (Pubitemid 19264376)
52. R.P. McEver, and R.D. Cummings Role of psgl-1 binding to selectins in leukocyte recruitment J Clin Invest 100 1997 S97 S103 (Pubitemid 28009555)
53. D.I. Simon, Z. Chen, and H. Xu Platelet glycoprotein ibalpha is a counterreceptor for the leukocyte integrin Mac-1 (CD11b/CD18) J Exp Med 192 2000 193 204 (Pubitemid 30470302)
54. T.G. Diacovo, S.J. Roth, J.M. Buccola, D.F. Bainton, and T.A. Springer Neutrophil rolling, arrest, and transmigration across activated, surface-adherent platelets via sequential action of P-selectin and the beta 2-integrin CD11b/CD18 Blood 88 1996 146 157 (Pubitemid 26230682)
55. C. Rogers, E.R. Edelman, and D.I. Simon A mAb to the beta2-leukocyte integrin Mac-1 (CD11b/CD18) reduces intimal thickening after angioplasty or stent implantation in rabbits Proc Natl Acad Sci U S A 95 1998 10134 10139 (Pubitemid 28415307)
56. D.I. Simon, Z. Dhen, P. Seifert, E.R. Edelman, C.M. Ballantyne, and C. Rogers Decreased neointimal formation in Mac-1(-/-) mice reveals a role for inflammation in vascular repair after angioplasty J Clin Invest 105 2000 293 300 (Pubitemid 30094449)
57. T. Inoue, Y. Sakai, K. Hoshi, I. Yaguchi, T. Fujito, and S. Morooka Lower expression of neutrophil adhesion molecule indicates less vessel wall injury and might explain lower restenosis rate after cutting balloon angioplasty Circulation 97 1998 2511 2518 (Pubitemid 28294497)
58. T. Inoue, Y. Sakai, S. Morooka, T. Hayashi, K. Takayanagi, and Y. Takabatake Expression of polymorphonuclear leukocyte adhesion molecules and its clinical significance in patients treated with percutaneous transluminal coronary angioplasty J Am Coll Cardiol 28 1996 1127 1133 (Pubitemid 26376984)
59. T. Inoue, R. Sohma, T. Miyazaki, Y. Iwasaki, I. Yaguchi, and S. Morooka Comparison of activation process of platelets and neutrophils after coronary stent implantation versus balloon angioplasty for stable angina pectoris Am J Cardiol 86 2000 1057 1062
60. T. Inoue, T. Uchida, I. Yaguchi, Y. Sakai, K. Takayanagi, and S. Morooka Stent-induced expression and activation of the leukocyte integrin Mac-1 is associated with neointimal thickening and restenosis Circulation 107 2003 1757 1763 (Pubitemid 36418356)
61. T. Asahara, T. Murohara, and A. Sullivan Isolation of putative progenitor endothelial cells for angiogenesis Science 275 1997 964 966
62. T. Murohara, H. Ikeda, and J. Duan Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization J Clin Invest 105 2000 1527 1536 (Pubitemid 30390303)
63. M. Sata, A. Saiura, and A. Kunisato Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis Nat Med 8 2002 403 409 (Pubitemid 34407037)
64. N.M. Caplice, T.J. Bunch, and P.G. Stalboerger Smooth muscle cells in human coronary atherosclerosis can originate from cells administered at marrow transplantation Proc Natl Acad Sci U S A 100 2003 4754 4759 (Pubitemid 36457802)
65. B.H. Strauss, D.C. MacLeod, and P.J. de Feyter Analysis of VNTR loci amplified by the polymerase chain reaction for investigating the origin of intimal smooth muscle cells in a coronary artery lesion developing after heart transplantation in man Am Heart J 125 1993 1176 1180 (Pubitemid 23117361)
66. A. Kawamoto, H.C. Gwon, and H. Iwaguro Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia Circulation 103 2001 634 637 (Pubitemid 32144189)
67. S. Shintani, T. Murohara, and H. Ikeda Mobilization of endothelial progenitor cells in patients with acute myocardial infarction Circulation 103 2001 2776 2779 (Pubitemid 32550062)
68. A. Schober, R. Hoffmann, and N. Oprée Peripheral cd34+ cells and the risk of in-stent restenosis in patients with coronary heart disease Am J Cardiol 96 2005 1116 1122 (Pubitemid 41416606)
69. T. Inoue, M. Sata, and Y. Hikichi Mobilization of cd34-positive bone marrow-derived cells after coronary stent implantation: impact on restenosis Circulation 115 2007 553 561 (Pubitemid 46226164)
70. G.S. Elemer, and T.S. Edgington Two independent sets of monoclonal antibodies define neoepitopes linked to soluble ligand binding and leukocyte adhesion functions of activated alpha M beta 2 Circ Res 75 1994 165 171
71. D. Fukuda, M. Sata, K. Tanaka, and R. Nagai Potent inhibitory effect of sirolimus on circulating vascular progenitor cells Circulation 111 2005 926 931 (Pubitemid 40279896)
72. T. Imanishi, K. Kobayashi, S. Kuki, C. Takahashi, and T. Akasaka Sirolimus accelerates senescence of endothelial progenitor cells through telomerase inactivation Atherosclerosis 189 2006 288 296 (Pubitemid 44634491)
73. X. Chen, S.E. Kelemen, and M.V. Autieri Expression of granulocyte colony-stimulating factor is induced in injured rat carotid arteries and mediates vascular smooth muscle cell migration Am J Physiol Cell Physiol 288 2005 C81 C88 (Pubitemid 39658430)
74. D. Zohlnhöfer, I. Ott, and J. Mehilli Stem cell mobilization by granulocyte colony-stimulating factor in patients with acute myocardial infarction: a randomized controlled trial JAMA 295 2006 1003 1010
75. H.J. Kang, H.S. Kim, and S.Y. Zhang Effects of intracoronary infusion of peripheral blood stem-cells mobilised with granulocyte-colony stimulating factor on left ventricular systolic function and restenosis after coronary stenting in myocardial infarction: the magic cell randomised clinical trial Lancet 363 2004 751 756
76. S. Starckx, P.E. Van den Steen, A. Wuyts, J. Van Damme, and G. Opdenakker Neutrophil gelatinase B and chemokines in leukocytosis and stem cell mobilization Leuk Lymphoma 43 2002 233 241 (Pubitemid 34202100)
77. J. Wize, I. Sopata, A. Smerdel, and S. Maliski Ligation of selectin L and integrin CD11b/CD18 (Mac-1) induces release of gelatinase B (MMP-9) from human neutrophils Inflamm Res 47 1998 325 327 (Pubitemid 28425162)
78. B. Heissig, K. Hattori, and S. Dias Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand Cell 109 2002 625 637 (Pubitemid 34628725)
79. L.M. Pelus, H. Bian, A.G. King, and S. Fukuda Neutrophil-derived MMP-9 mediates synergistic mobilization of hematopoietic stem and progenitor cells by the combination of G-CSF and the chemokines GRObeta/CXCL2 and GRObetaT/CXCL2delta4 Blood 103 2004 110 119 (Pubitemid 38029925)
80. A. Schober, S. Knarren, M. Lietz, E.A. Lin, and C. Weber Crucial role of stromal cell-derived factor-1alpha in neointima formation after vascular injury in apolipoprotein e-deficient mice Circulation 108 2003 2491 2497 (Pubitemid 37444411)
81. J. Folkman Angiogenesis in cancer, vascular, rheumatoid and other disease Nat Med 1 1995 27 31
82. D.H. Walter, M. Cejna, and L. Diaz-Sandoval Local gene transfer of phvegf-2 plasmid by gene-eluting stents: an alternative strategy for inhibition of restenosis Circulation 110 2004 36 45 (Pubitemid 38885702)
83. M.J. Kutryk, and M.A. Kuliszewski In vivo endothelial progenitor cell seeding for the accelerated endothelialization of endovascular devices Am J Cardiol 92 2003 94 98
84. R. Blindt, F. Vogt, and I. Astafieva A novel drug-eluting stent coated with an integrin-binding cyclic Arg-Gly-Asp peptide inhibits neointimal hyperplasia by recruiting endothelial progenitor cells J Am Coll Cardiol 47 2006 1786 1795
85. J. Aoki, P.W. Serruys, and H. van Beusekom Endothelial progenitor cell capture by stents coated with antibody against CD34: the Healing-FIM (Healthy Endothelial Accelerated Lining Inhibits Neointimal Growth-First in Man) Registry J Am Coll Cardiol 45 2005 1574 1579 (Pubitemid 40704488)
86. M. Miglionico, G. Patti, A. D'Ambrosio, and G. Di Sciascio Percutaneous coronary intervention utilizing a new endothelial progenitor cells antibody-coated stent: a prospective single-center registry in high-risk patients Catheter Cardiovasc Interv 71 2008 600 604 (Pubitemid 351550395)
87. B. Assmus, C. Urbich, and A. Aicher HMG-CoA reductase inhibitors reduce senescence and increase proliferation of endothelial progenitor cells via regulation of cell cycle regulatory genes Circ Res 92 2003 1049 1055 (Pubitemid 36588505)
88. M. Vasa, S. Fichtlscherer, and K. Adler Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease Circulation 103 2001 2885 2890 (Pubitemid 32578123)
89. W.K. den Dekker, J.H. Houtgraaf, and Y. Onuma Final results of the HEALING IIB trial to evaluate a bio-engineered CD34 antibody coated stent (Genous™Stent) designed to promote vascular healing by capture of circulating endothelial progenitor cells in CAD patients Atherosclerosis 2011 Jun 25 10.1016/j.atherosclerosis.2011.06.032 [E-pub ahead of print]
90. C. Gensch, Y.P. Clever, C. Werner, M. Hanhoun, M. Böhm, and U. Laufs The PPAR-gamma agonist pioglitazone increases neoangiogenesis and prevents apoptosis of endothelial progenitor cells Atherosclerosis 192 2007 67 74 (Pubitemid 46628806)