Vein graft failure: From pathophysiology to clinical outcomes

Nature Reviews Cardiology

Volumn 13, Issue 8, 2016, Pages 451-470

  De Vries, Margreet R ^a   Simons, Karin H ^a   Jukema, J Wouter ^a   Braun, Jerry ^a   Quax, Paul H A ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; ACETYLSALICYLIC ACID PLUS DIPYRIDAMOLE; ANTICOAGULANT AGENT; ANTILIPEMIC AGENT; ANTITHROMBOCYTIC AGENT; CHOLESTEROL; CLOPIDOGREL; CYTOKINE; FIBRIN; GROWTH FACTOR; INDOBUFEN; OLIGONUCLEOTIDE; TICAGRELOR; TRANSCRIPTION FACTOR E2F;

ADVENTITIA; ANGIOGENESIS; ANTICOAGULANT THERAPY; APOPTOSIS; ARTERY INTIMA; ATHEROSCLEROSIS; BYPASS SURGERY; CELL PROLIFERATION; ENDOSCOPIC SURGERY; ENDOTHELIUM; FIBROBLAST; GRAFT FAILURE; GRAFT PATENCY; HUMAN; HYPERPLASIA; INFLAMMATORY CELL; LYMPHOCYTE; MONOCYTE; NEUTROPHIL; NONHUMAN; OUTCOME ASSESSMENT; PATHOPHYSIOLOGY; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; REVIEW; SMOOTH MUSCLE CELL; THROMBOSIS; TISSUE PRESERVATION; VEIN GRAFT; VEIN GRAFT DISEASE; VEIN RUPTURE; VEIN TRANSPLANTATION; ANIMAL; BIOPSY; COMPUTED TOMOGRAPHIC ANGIOGRAPHY; CORONARY ANGIOGRAPHY; CORONARY ARTERY BYPASS GRAFT; CORONARY ARTERY DISEASE; DIAGNOSTIC IMAGING; GRAFT OCCLUSION; PERCUTANEOUS TRANSLUMINAL ANGIOPLASTY; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PROCEDURES; REOPERATION; RISK FACTOR; SAPHENOUS VEIN; TRANSPLANTATION; TREATMENT FAILURE; VASCULAR PATENCY;

ANGIOPLASTY, BALLOON; ANIMALS; BIOPSY; COMPUTED TOMOGRAPHY ANGIOGRAPHY; CORONARY ANGIOGRAPHY; CORONARY ARTERY BYPASS; CORONARY ARTERY DISEASE; GRAFT OCCLUSION, VASCULAR; HUMANS; PERIPHERAL ARTERIAL DISEASE; REOPERATION; RISK FACTORS; SAPHENOUS VEIN; TREATMENT FAILURE; VASCULAR PATENCY;

EID: 84969593683     PISSN: 17595002     EISSN: 17595010     Source Type: Journal    
DOI: 10.1038/nrcardio.2016.76     Document Type: Review

References (314)

1. Weintraub, W. S. et al. Comparative effectiveness of revascularization strategies. N. Engl. J. Med. 366, 1467-1476 (2012).
2. Deb, S. et al. Coronary artery bypass graft surgery versus percutaneous interventions in coronary revascularization: A systematic review. JAMA 310, 2086-2095 (2013).
3. Owens, C. D. Adaptive changes in autogenous vein grafts for arterial reconstruction: Clinical implications. J. Vasc. Surg. 51, 736-746 (2010).
4. Windecker, S. et al. 2014 ESC/EACTS Guidelines on myocardial revascularization: The Task Force on Myocardial Revascularization of the European Society of Cardiology (ESC) and the European Association for Cardio-Thoracic Surgery (EACTS). Developed with the special contribution of the European Association of Percutaneous Cardiovascular Interventions (EAPCI). Eur. Heart J. 35, 2541-2619 (2014).
5. Goldman, S. et al. Long-term patency of saphenous vein and left internal mammary artery grafts after coronary artery bypass surgery: Results from a Department of Veterans Affairs Cooperative Study. J. Am. Coll. Cardiol. 44, 2149-2156 (2004).
6. Carrel, A., Guthrie, C. C. Uniterminal and biterminal venous transplantations. Surg. Gynecol. Obstet. 266-286 (1906).
7. Walts, A. E., Fishbein, M. C., Matloff, J. M. Thrombosed, ruptured atheromatous plaques in saphenous vein coronary artery bypass grafts: Ten years' experience. Am. Heart J. 114, 718-723 (1987).
8. Motwani, J. G., Topol, E. J. Aortocoronary saphenous vein graft disease: Pathogenesis, predisposition, and prevention. Circulation 97, 916-931 (1998).
9. Yanagawa, B. et al. Clinical, biochemical, and genetic predictors of coronary artery bypass graft failure. J. Thorac. Cardiovasc. Surg. 148, 515-520 (2014).
10. Kulik, A., Ruel, M. Statins and coronary artery bypass graft surgery: Preoperative and postoperative efficacy and safety. Expert. Opin. Drug Saf. 8, 559-571 (2009).
11. Christenson, J. T. Preoperative lipid control with simvastatin reduces the risk for graft failure already 1 year after myocardial revascularization. Cardiovasc. Surg. 9, 33-43 (2001).
12. Efird, J. T. et al. Implications of hemodialysis in patients undergoing coronary artery bypass grafting. Int. J. Cardiovasc. Res. 2, 1000154 (2013).
13. Conte, M. S. et al. Risk factors, medical therapies and perioperative events in limb salvage surgery: Observations from the PREVENT III multicenter trial. J. Vasc. Surg. 42, 456-464 (2005).
14. Monahan, T. S., Owens, C. D. Risk factors for lower-extremity vein graft failure. Semin. Vasc. Surg. 22, 216-226 (2009).
15. Owens, C. D., Ho, K. J., Conte, M. S. Risk factors for failure of lower-extremity revascularization procedures: Are they different for bypass and percutaneous procedures Semin. Vasc. Surg. 21, 143-153 (2008).
16. Kon, Z. N. et al. The role of preexisting pathology in the development of neointimal hyperplasia in coronary artery bypass grafts. J. Surg. Res. 142, 351-356 (2007).
17. Perek, B. et al. Predictive factors of late venous aortocoronary graft failure: Ultrastructural studies. PLoS ONE 8, e70628 (2013).
18. Hess, C. N. et al. Saphenous vein graft failure after coronary artery bypass surgery: Insights from PREVENT IV. Circulation 130, 1445-1451 (2014).
19. Hillis, L. D. et al. 2011 ACCF/AHA Guideline for Coronary Artery Bypass Graft Surgery: A report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. Circulation 124, e652-e735 (2011).
20. Tendera, M. et al. ESC guidelines on the diagnosis and treatment of peripheral artery diseases: Document covering atherosclerotic disease of extracranial carotid and vertebral, mesenteric, renal, upper and lower extremity arteries: The Task Force on the Diagnosis and Treatment of Peripheral Artery Diseases of the European Society of Cardiology (ESC). Eur. Heart J. 32, 2851-2906 (2011).
21. Anderson, J. L. et al. Management of patients with peripheral artery disease (compilation of 2005 and 2011 ACCF/AHA guideline recommendations): A report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. Circulation 127, 1425-1443 (2013).
22. Wan, S., George, S. J., Berry, C., Baker, A. H. Vein graft failure: Current clinical practice and potential for gene therapeutics. Gene Ther. 19, 630-636 (2012).
23. Lardenoye, J. H. et al. Accelerated atherosclerosis and calcification in vein grafts: A study in APOE 3 Leiden transgenic mice. Circ. Res. 91, 577-584 (2002).
24. Owens, C. D. et al. Early biomechanical changes in lower extremity vein grafts-distinct temporal phases of remodeling and wall stiffness. J. Vasc. Surg. 44, 740-746 (2006).
25. de Vries, M. R. et al. Plaque rupture complications in murine atherosclerotic vein grafts can be prevented by TIMP-1 overexpression. PLoS ONE 7, e47134 (2012).
26. Yahagi, K. et al. Pathophysiology of native coronary, vein graft, and in-stent atherosclerosis. Nat. Rev. Cardiol. 13, 79-98 (2016).
27. Kwei, S. et al. Early adaptive responses of the vascular wall during venous arterialization in mice. Am. J. Pathol. 164, 81-89 (2004).
28. Weaver, H., Shukla, N., Ellinsworth, D., Jeremy, J. Y. Oxidative stress and vein graft failure: A focus on NADH oxidase, nitric oxide and eicosanoids. Curr. Opin. Pharmacol. 12, 160-165 (2012).
29. Osgood, M. J. et al. Surgical vein graft preparation promotes cellular dysfunction, oxidative stress, and intimal hyperplasia in human saphenous vein. J. Vasc. Surg. 60, 202-211 (2014).
30. Westerband, A. et al. Vein adaptation to arterialization in an experimental model. J. Vasc. Surg. 33, 561-569 (2001).
31. Borin, T. F. et al. Apoptosis, cell proliferation and modulation of cyclin-dependent kinase inhibitor p21cip1 in vascular remodelling during vein arterialization in the rat. Int. J. Exp. Pathol. 90, 328-337 (2009).
32. Ehsan, A. et al. Endothelial healing in vein grafts: Proliferative burst unimpaired by genetic therapy of neointimal disease. Circulation 105, 1686-1692 (2002).
33. Sugimoto, M., Yamanouchi, D., Komori, K. Therapeutic approach against intimal hyperplasia of vein grafts through endothelial nitric oxide synthase/nitric oxide (eNOS/NO) and the Rho/Rho-kinase pathway. Surg. Today 39, 459-465 (2009).
34. Shi, Y. et al. Oxidative stress and lipid retention in vascular grafts: Comparison between venous and arterial conduits. Circulation 103, 2408-2413 (2001).
35. Komori, K., Inoguchi, H., Kume, M., Shoji, T., Furuyama, T. Differences in endothelial function and morphologic modulation between canine autogenous venous and arterial grafts: Endothelium and intimal thickening. Surgery 131, S249-S255 (2002).
36. Tseng, C. N. et al. Contribution of endothelial injury and inflammation in early phase to vein graft failure: The causal factors impact on the development of intimal hyperplasia in murine models. PLoS ONE 9, e98904 (2014).
37. Yukizane, T., Okadome, K., Eguchi, H., Muto, Y., Sugimachi, K. Isotopic study of the effects of platelets on development of intimal thickening in autologous vein grafts in dogs. Br. J. Surg. 78, 297-302 (1991).
38. Lievens, D. et al. Platelet CD40L mediates thrombotic and inflammatory processes in atherosclerosis. Blood 116, 4317-4327 (2010).
39. Depta, J. P., Bhatt, D. L. New approaches to inhibiting platelets and coagulation. Annu. Rev. Pharmacol. Toxicol. 55, 373-397 (2015).
40. Cerrato, R. et al. Endothelin-1 increases superoxide production in human coronary artery bypass grafts. Life Sci. 91, 723-728 (2012).
41. West, N. E. et al. Nitric oxide synthase (nNOS) gene transfer modifies venous bypass graft remodeling: Effects on vascular smooth muscle cell differentiation and superoxide production. Circulation 104, 1526-1532 (2001).
42. Hattori, K. et al. Celiprolol reduces the intimal thickening of autogenous vein grafts via an enhancement of nitric oxide function through an inhibition of superoxide production. J. Vasc. Surg. 46, 116-123 (2007).
43. Zou, Y. et al. Mouse model of venous bypass graft arteriosclerosis. Am. J. Pathol. 153, 1301-1310 (1998).
44. Owens, C. D., Wake, N., Conte, M. S., Gerhard-Herman, M., Beckman, J. A. In vivo human lower extremity saphenous vein bypass grafts manifest flow mediated vasodilation. J. Vasc. Surg. 50, 1063-1070 (2009).
45. Hu, Y. et al. Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. J. Clin. Invest. 113, 1258-1265 (2004).
46. Diao, Y., Xue, J., Segal, M. S. A novel mouse model of autologous venous graft intimal hyperplasia. J. Surg. Res. 126, 106-113 (2005).
47. Torsney, E., Hu, Y., Xu, Q. Adventitial progenitor cells contribute to arteriosclerosis. Trends Cardiovasc. Med. 15, 64-68 (2005).
48. Brown, M. A. et al. Human umbilical cord blood-derived endothelial cells reendothelialize vein grafts and prevent thrombosis. Arterioscler. Thromb. Vasc. Biol. 30, 2150-2155 (2010).
49. Watson, A. R. et al. Deficiency of bone marrow 3-integrin enhances non-functional neovascularization. J. Pathol. 220, 435-445 (2010).
50. Liang, M. et al. Impaired integrin 3 delays endothelial cell regeneration and contributes to arteriovenous graft failure in mice. Arterioscler. Thromb. Vasc. Biol. 35, 607-615 (2015).
51. Wong, M. M. et al. Macrophages control vascular stem/progenitor cell plasticity through tumor necrosis factor-mediated nuclear factor-B activation. Arterioscler. Thromb. Vasc. Biol. 34, 635-643 (2014).
52. Mayr, U. et al. Accelerated arteriosclerosis of vein grafts in inducible NO synthase/mice is related to decreased endothelial progenitor cell repair. Circ. Res. 98, 412-420 (2006).
53. Johnson, T. R., Tomaszewski, J. E., Carpenter, J. P. Cellular repopulation of human vein allograft bypass grafts. J. Vasc. Surg. 31, 994-1002 (2000).
54. Szilagyi, D. E., Smith, R. F., Elliott, J. P. Venous autografts in femoropolpitieal arterioplasty. Obervations in the treatment of occlusive disease. Arch. Surg. 89, 113-125 (1964).
55. Owens, C. D., Ho, K. J., Conte, M. S. Lower extremity vein graft failure: A translational approach. Vasc. Med. 13, 63-74 (2008).
56. Dashwood, M. R., Tsui, J. C. 'No-touch' saphenous vein harvesting improves graft performance in patients undergoing coronary artery bypass surgery: A journey from bedside to bench. Vascul. Pharmacol. 58, 240-250 (2013).
57. Chiu, J. J., Chien, S. Effects of disturbed flow on vascular endothelium: Pathophysiological basis and clinical perspectives. Physiol. Rev. 91, 327-387 (2011).
58. Berard, X. et al. Role of hemodynamic forces in the ex vivo arterialization of human saphenous veins. J. Vasc. Surg. 57, 1371-1382 (2013).
59. Dobrin, P. B., Littooy, F. N., Endean, E. D. Mechanical factors predisposing to intimal hyperplasia and medial thickening in autogenous vein grafts. Surgery 105, 393-400 (1989).
60. Meyerson, S. L. et al. The effects of extremely low shear stress on cellular proliferation and neointimal thickening in the failing bypass graft. J. Vasc. Surg. 34, 90-97 (2001).
61. Zilla, P. et al. Remodeling leads to distinctly more intimal hyperplasia in coronary than in infrainguinal vein grafts. J. Vasc. Surg. 55, 1734-1741 (2012).
62. Murphy, G. J., Angelini, G. D. Insights into the pathogenesis of vein graft disease: Lessons from intravascular ultrasound. Cardiovasc. Ultrasound 2, 8 (2004).
63. Hong, Y. J. et al. Disease progression in nonintervened saphenous vein graft segments a serial intravascular ultrasound analysis. J. Am. Coll. Cardiol. 53, 1257-1264 (2009).
64. Wong, A. P. et al. Expansive remodeling in venous bypass grafts: Novel implications for vein graft disease. Atherosclerosis 196, 580-589 (2008).
65. Mavromatis, K. et al. Early effects of arterial hemodynamic conditions on human saphenous veins perfused ex vivo. Arterioscler. Thromb. Vasc. Biol. 20, 1889-1895 (2000).
66. McCabe, M., Cunningham, G. J., Wyatt, A. P., Rothnie, N. G., Taylor, G. W. A histological and histochemical examination of autogenous vein grafts. Br. J. Surg. 54, 147-155 (1967).
67. Glagov, S., Weisenberg, E., Zarins, C. K., Stankunavicius, R., Kolettis, G. J. Compensatory enlargement of human atherosclerotic coronary arteries. N. Engl. J. Med. 316, 1371-1375 (1987).
68. Lau, G. T. et al. Lumen loss in the first year in saphenous vein grafts is predominantly a result of negative remodeling of the whole vessel rather than a result of changes in wall thickness. Circulation 114, I435-I440 (2006).
69. Gasper, W. J. et al. Thirty-day vein remodeling is predictive of midterm graft patency after lower extremity bypass. J. Vasc. Surg. 57, 9-18 (2013).
70. Izzat, M. B. et al. Influence of external stent size on early medial and neointimal thickening in a pig model of saphenous vein bypass grafting. Circulation 94, 1741-1745 (1996).
71. Angelini, G. D., Lloyd, C., Bush, R., Johnson, J., Newby, A. C. An external, oversized, porous polyester stent reduces vein graft neointima formation, cholesterol concentration, and vascular cell adhesion molecule 1 expression in cholesterol-fed pigs. J. Thorac. Cardiovasc. Surg. 124, 950-956 (2002).
72. Lardenoye, J. H. et al. Inhibition of accelerated atherosclerosis in vein grafts by placement of external stent in apoE∗3-Leiden transgenic mice. Arterioscler. Thromb. Vasc. Biol. 22, 1433-1438 (2002).
73. Moodley, L. et al. Protective constriction of coronary vein grafts with knitted nitinol. Eur. J. Cardiothorac. Surg. 44, 64-71 (2013).
74. Longchamp, A. et al. The use of external mesh reinforcement to reduce intimal hyperplasia and preserve the structure of human saphenous veins. Biomaterials 35, 2588-2599 (2014).
75. Kalra, M., Miller, V. M. Early remodeling of saphenous vein grafts: Proliferation, migration and apoptosis of adventitial and medial cells occur simultaneously with changes in graft diameter and blood flow. J. Vasc. Res. 37, 576-584 (2000).
76. Mitra, A. K., Gangahar, D. M., Agrawal, D. K. Cellular, molecular and immunological mechanisms in the pathophysiology of vein graft intimal hyperplasia. Immunol. Cell Biol. 84, 115-124 (2006).
77. Jiang, Z. et al. Established neointimal hyperplasia in vein grafts expands via TGF-mediated progressive fibrosis. Am. J. Physiol. Heart Circ. Physiol. 297, H1200-H1207 (2009).
78. Kenagy, R. D. et al. Proliferative capacity of vein graft smooth muscle cells and fibroblasts in vitro correlates with graft stenosis. J. Vasc. Surg. 49, 1282-1288 (2009).
79. Jin, D. et al. Outside fibroblasts play a key role in the development of inner neointima after the implantation of polytetrafluoroethylene grafts. J. Pharmacol. Sci. 119, 139-149 (2012).
80. Zhang, L., Freedman, N. J., Brian, L., Peppel, K. Graft-extrinsic cells predominate in vein graft arterialization. Arterioscler. Thromb. Vasc. Biol. 24, 470-476 (2004).
81. Diao, Y. et al. Long-term engraftment of bone marrow-derived cells in the intimal hyperplasia lesion of autologous vein grafts. Am. J. Pathol. 172, 839-848 (2008).
82. Psaltis, P. J., Harbuzariu, A., Delacroix, S., Holroyd, E. W., Simari, R. D. Resident vascular progenitor cells-diverse origins, phenotype, and function. J. Cardiovasc. Transl. Res. 4, 161-176 (2011).
83. Jevon, M. et al. Smooth muscle cells in porcine vein graft intimal hyperplasia are derived from the local vessel wall. Cardiovasc. Pathol. 20, e91-e94 (2011).
84. Chen, Y. et al. Adventitial stem cells in vein grafts display multilineage potential that contributes to neointimal formation. Arterioscler. Thromb. Vasc. Biol. 33, 1844-1851 (2013).
85. Liang, M., Liang, A., Wang, Y., Jiang, J., Cheng, J. Smooth muscle cells from the anastomosed artery are the major precursors for neointima formation in both artery and vein grafts. Basic Res. Cardiol. 109, 431 (2014).
86. Iwata, H. et al. Bone marrow-derived cells contribute to vascular inflammation but do not differentiate into smooth muscle cell lineages. Circulation 122, 2048-2057 (2010).
87. Zhang, L., Brian, L., Freedman, N. J. Vein graft neointimal hyperplasia is exacerbated by CXCR4 signaling in vein graft-extrinsic cells. J. Vasc. Surg. 56, 1390-1397 (2012).
88. Cheng, J., Wang, Y., Liang, A., Jia, L., Du, J. FSP-1 silencing in bone marrow cells suppresses neointima formation in vein graft. Circ. Res. 110, 230-240 (2012).
89. Woodside, K. J. et al. Altered expression of vascular endothelial growth factor and its receptors in normal saphenous vein and in arterialized and stenotic vein grafts. Am. J. Surg. 186, 561-568 (2003).
90. Sterpetti, A. V. et al. Progression and regression of myointimal hyperplasia in experimental vein grafts depends on platelet-derived growth factor and basic fibroblastic growth factor production. J. Vasc. Surg. 23, 568-575 (1996).
91. Friedl, R. et al. Intimal hyperplasia and expression of transforming growth factor-1 in saphenous veins and internal mammary arteries before coronary artery surgery. Ann. Thorac. Surg. 78, 1312-1318 (2004).
92. You, W. J., Xiao, M. D., Yuan, Z. X. Significance of changes in transforming growth factor-mRNA levels in autogenous vein grafts. Chin. Med. J. (Engl.) 117, 1060-1065 (2004).
93. Jeremy, J. Y., Shukla, N., Angelini, G. D., Wan, S. Endothelin-1 (ET-1) and vein graft failure and the therapeutic potential of ET-1 receptor antagonists. Pharmacol. Res. 63, 483-489 (2011).
94. Luo, Z., Asahara, T., Tsurumi, Y., Isner, J. M., Symes, J. F. Reduction of vein graft intimal hyperplasia and preservation of endothelium-dependent relaxation by topical vascular endothelial growth factor. J. Vasc. Surg. 27, 167-173 (1998).
95. Hu, Y., Zou, Y., Dietrich, H., Wick, G., Xu, Q. Inhibition of neointima hyperplasia of mouse vein grafts by locally applied suramin. Circulation 100, 861-868 (1999).
96. Kimura, S. et al. Local delivery of imatinib mesylate (STI571)-incorporated nanoparticle ex vivo suppresses vein graft neointima formation. Circulation 118, S65-S70 (2008).
97. Kapur, N. K. et al. Inhibition of transforming growth factor-restores endothelial thromboresistance in vein grafts. J. Vasc. Surg. 54, 1117-1123 (2011).
98. Sun, D. X. et al. Nanoparticle-mediated local delivery of an antisense TGF-1 construct inhibits intimal hyperplasia in autogenous vein grafts in rats. PLoS ONE 7, e41857 (2012).
99. Yang, Z. et al. Different proliferative properties of smooth muscle cells of human arterial and venous bypass vessels: Role of PDGF receptors, mitogen-activated protein kinase, and cyclin-dependent kinase inhibitors. Circulation 97, 181-187 (1998).
100. Saunders, P. C. et al. Vein graft arterialization causes differential activation of mitogen-activated protein kinases. J. Thorac. Cardiovasc. Surg. 127, 1276-1284 (2004).
101. Chanakira, A. et al. Hypoxia differentially regulates arterial and venous smooth muscle cell migration. PLoS ONE 10, e0138587 (2015).
102. Ge, J. J. et al. p38 MAPK inhibitor, CBS3830 limits vascular remodelling in arterialised vein grafts. Heart Lung Circ. 22, 751-758 (2013).
103. Turner, N. A., Ho, S., Warburton, P., O'Regan, D. J., Porter, K. E. Smooth muscle cells cultured from human saphenous vein exhibit increased proliferation, invasion, and mitogen-activated protein kinase activation in vitro compared with paired internal mammary artery cells. J. Vasc. Surg. 45, 1022-1028 (2007).
104. Weiss, S. et al. Different migration of vascular smooth muscle cells from human coronary artery bypass vessels. Role of Rho/ROCK pathway. J. Vasc. Res. 44, 149-156 (2007).
105. Li, P. et al. Cross talk between vascular smooth muscle cells and monocytes through interleukin-1/interleukin-18 signaling promotes vein graft thickening. Arterioscler. Thromb. Vasc. Biol. 34, 2001-2011 (2014).
106. Frischknecht, K. et al. Different vascular smooth muscle cell apoptosis in the human internal mammary artery and the saphenous vein. Implications for bypass graft disease. J. Vasc. Res. 43, 338-346 (2006).
107. Berceli, S. A. et al. Differential expression and activity of matrix metalloproteinases during flow-modulated vein graft remodeling. J. Vasc. Surg. 39, 1084-1090 (2004).
108. Sharony, R. et al. Matrix metalloproteinase expression in vein grafts: Role of inflammatory mediators and extracellular signal-regulated kinases-1 and-2. Am. J. Physiol. Heart Circ. Physiol. 290, H1651-H1659 (2006).
109. Lardenoye, J. H. et al. Inhibition of intimal hyperplasia by the tetracycline derived mmp inhibitor doxycycline in vein graft disease in vitro and in vivo. EuroIntervention 1, 236-243 (2005).
110. Perek, B. et al. Preexisting high expression of matrix metalloproteinase-2 in tunica media of saphenous vein conduits is associated with unfavorable long-term outcomes after coronary artery bypass grafting. Biomed. Res. Int. 2013, 730721 (2013).
111. Turner, N. A., Hall, K. T., Ball, S. G., Porter, K. E. Selective gene silencing of either MMP-2 or MMP-9 inhibits invasion of human saphenous vein smooth muscle cells. Atherosclerosis 193, 36-43 (2007).
112. Thomas, A. C., Newby, A. C. Effect of matrix metalloproteinase-9 knockout on vein graft remodelling in mice. J. Vasc. Res. 47, 299-308 (2010).
113. George, S. J., Baker, A. H., Angelini, G. D., Newby, A. C. Gene transfer of tissue inhibitor of metalloproteinase-2 inhibits metalloproteinase activity and neointima formation in human saphenous veins. Gene Ther. 5, 1552-1560 (1998).
114. George, S. J., Johnson, J. L., Angelini, G. D., Newby, A. C., Baker, A. H. Adenovirus-mediated gene transfer of the human TIMP-1 gene inhibits smooth muscle cell migration and neointimal formation in human saphenous vein. Hum. Gene Ther. 9, 867-877 (1998).
115. George, S. J., Lloyd, C. T., Angelini, G. D., Newby, A. C., Baker, A. H. Inhibition of late vein graft neointima formation in human and porcine models by adenovirus-mediated overexpression of tissue inhibitor of metalloproteinase-3. Circulation 101, 296-304 (2000).
116. Hu, Y., Baker, A. H., Zou, Y., Newby, A. C., Xu, Q. Local gene transfer of tissue inhibitor of metalloproteinase-2 influences vein graft remodeling in a mouse model. Arterioscler. Thromb. Vasc. Biol. 21, 1275-1280 (2001).
117. George, S. J. et al. Sustained reduction of vein graft neointima formation by ex vivo TIMP-3 gene therapy. Circulation 124, S135-S142 (2011).
118. Wolff, R. A. et al. Antisense to transforming growth factor-1 messenger RNA reduces vein graft intimal hyperplasia and monocyte chemotactic protein 1. J. Vasc. Surg. 41, 498-508 (2005).
119. van den Boom, M. et al. Differential regulation of hyaluronic acid synthase isoforms in human saphenous vein smooth muscle cells: Possible implications for vein graft stenosis. Circ. Res. 98, 36-44 (2006).
120. Kauhanen, P. et al. Plasminogen activator inhibitor-1 in neointima of vein grafts: Its role in reduced fibrinolytic potential and graft failure. Circulation 96, 1783-1789 (1997).
121. Siren, V. et al. Urokinase, tissue-type plasminogen activator and plasminogen activator inhibitor-1 expression in severely stenosed and occluded vein grafts with thrombosis. Blood Coagul. Fibrinolysis 14, 369-377 (2003).
122. Fay, W. P., Garg, N., Sunkar, M. Vascular functions of the plasminogen activation system. Arterioscler. Thromb. Vasc. Biol. 27, 1231-1237 (2007).
123. Carmeliet, P. et al. Urokinase but not tissue plasminogen activator mediates arterial neointima formation in mice. Circ. Res. 81, 829-839 (1997).
124. Thomas, A. C., Wyatt, M. J., Newby, A. C. Reduction of early vein graft thrombosis by tissue plasminogen activator gene transfer. Thromb. Haemost. 102, 145-152 (2009).
125. Diebold, I., Kraicun, D., Bonello, S., Gorlach, A. The 'PAI-1 paradox' in vascular remodeling. Thromb. Haemost. 100, 984-991 (2008).
126. Ji, Y. et al. Multifaceted role of plasminogen activator inhibitor-1 in regulating early remodeling of vein bypass grafts. Arterioscler. Thromb. Vasc. Biol. 31, 1781-1787 (2011).
127. Lamfers, M. L. et al. Gene transfer of the urokinase-type plasminogen activator receptor-targeted matrix metalloproteinase inhibitor TIMP-1.ATF suppresses neointima formation more efficiently than tissue inhibitor of metalloproteinase-1. Circ. Res. 91, 945-952 (2002).
128. Eefting, D. et al. In vivo suppression of vein graft disease by nonviral, electroporation-mediated, gene transfer of tissue inhibitor of metalloproteinase-1 linked to the amino terminal fragment of urokinase (TIMP-1.ATF), a cell-surface directed matrix metalloproteinase inhibitor. J. Vasc. Surg. 51, 429-437 (2010).
129. Eefting, D. et al. A novel urokinase receptor-targeted inhibitor for plasmin and matrix metalloproteinases suppresses vein graft disease. Cardiovasc. Res. 88, 367-375 (2010).
130. Quax, P. H. et al. Adenoviral expression of a urokinase receptor-targeted protease inhibitor inhibits neointima formation in murine and human blood vessels. Circulation 103, 562-569 (2001).
131. Schepers, A. et al. Short-term dexamethasone treatment inhibits vein graft thickening in hypercholesterolemic ApoE3Leiden transgenic mice. J. Vasc. Surg. 43, 809-815 (2006).
132. Ozaki, C. K. Cytokines and the early vein graft: Strategies to enhance durability. J. Vasc. Surg. 45, A92-A98 (2007).
133. Piccinini, A. M., Midwood, K. S. DAMPening inflammation by modulating TLR signalling. Mediators. Inflamm. 2010, 672395 (2010).
134. Karper, J. C. et al. Toll-like receptor 4 is involved in human and mouse vein graft remodeling, and local gene silencing reduces vein graft disease in hypercholesterolemic APOE∗3Leiden mice. Arterioscler. Thromb. Vasc. Biol. 31, 1033-1040 (2011).
135. Khaleel, M. S. et al. High-pressure distention of the saphenous vein during preparation results in increased markers of inflammation: A potential mechanism for graft failure. Ann. Thorac. Surg. 93, 552-558 (2012).
136. Hollestelle, S. C. et al. Toll-like receptor 4 is involved in outward arterial remodeling. Circulation 109, 393-398 (2004).
137. Sobel, M. et al. Low levels of a natural IgM antibody are associated with vein graft stenosis and failure. J. Vasc. Surg. 58, 997-1005 (2013).
138. Faria-Neto, J. R. et al. Passive immunization with monoclonal IgM antibodies against phosphorylcholine reduces accelerated vein graft atherosclerosis in apolipoprotein E-null mice. Atherosclerosis 189, 83-90 (2006).
139. Kawai, T., Akira, S. The role of pattern-recognition receptors in innate immunity: Update on Toll-like receptors. Nat. Immunol. 11, 373-384 (2010).
140. Shintani, T. et al. Intraoperative transfection of vein grafts with the NFB decoy in a canine aortocoronary bypass model: A strategy to attenuate intimal hyperplasia. Ann. Thorac. Surg. 74, 1132-1137 (2002).
141. Miyake, T. et al. Inhibitory effects of NFB decoy oligodeoxynucleotides on neointimal hyperplasia in a rabbit vein graft model. J. Mol. Cell. Cardiol. 41, 431-440 (2006).
142. Meng, X. B. et al. Small interfering RNA targeting nuclear factor kappa B to prevent vein graft stenosis in rat models. Transplant. Proc. 45, 2553-2558 (2013).
143. Tatewaki, H. et al. Blockade of monocyte chemoattractant protein-1 by adenoviral gene transfer inhibits experimental vein graft neointimal formation. J. Vasc. Surg. 45, 1236-1243 (2007).
144. Fu, C. et al. Monocyte chemoattractant protein-1/CCR2 axis promotes vein graft neointimal hyperplasia through its signaling in graft-extrinsic cell populations. Arterioscler. Thromb. Vasc. Biol. 32, 2418-2426 (2012).
145. Schepers, A. et al. Anti-MCP-1 gene therapy inhibits vascular smooth muscle cells proliferation and attenuates vein graft thickening both in vitro and in vivo. Arterioscler. Thromb. Vasc. Biol. 26, 2063-2069 (2006).
146. Zhang, L., Peppel, K., Brian, L., Chien, L., Freedman, N. J. Vein graft neointimal hyperplasia is exacerbated by tumor necrosis factor receptor-1 signaling in graft-intrinsic cells. Arterioscler. Thromb. Vasc. Biol. 24, 2277-2283 (2004).
147. Zhang, L. et al. Tumor necrosis factor receptor-2 signaling attenuates vein graft neointima formation by promoting endothelial recovery. Arterioscler. Thromb. Vasc. Biol. 28, 284-289 (2008).
148. Faries, P. L. et al. Immunolocalization and temporal distribution of cytokine expression during the development of vein graft intimal hyperplasia in an experimental model. J. Vasc. Surg. 24, 463-471 (1996).
149. Sterpetti, A. V. et al. Formation of myointimal hyperplasia and cytokine production in experimental vein grafts. Surgery 123, 461-469 (1998).
150. Jiang, Z. et al. Wall shear modulation of cytokines in early vein grafts. J. Vasc. Surg. 40, 345-350 (2004).
151. Schepers, A. et al. Inhibition of complement component C3 reduces vein graft atherosclerosis in apolipoprotein E3-Leiden transgenic mice. Circulation 114, 2831-2838 (2006).
152. Krijnen, P. A. et al. C1-esterase inhibitor protects against early vein graft remodeling under arterial blood pressure. Atherosclerosis 220, 86-92 (2012).
153. de Vries, M. R. et al. Complement factor C5a as mast cell activator mediates vascular remodelling in vein graft disease. Cardiovasc. Res. 97, 311-320 (2013).
154. Smith, P. K. et al. Effects of C5 complement inhibitor pexelizumab on outcome in high-risk coronary artery bypass grafting: Combined results from the PRIMO-CABG I and II trials. J. Thorac. Cardiovasc. Surg. 142, 89-98 (2011).
155. Dashwood, M. R. Distension of the saphenous vein during graft preparation: Markers of inflammation or endothelium Ann. Thorac. Surg. 94, 2177-2178 (2012).
156. Schlitt, A. et al. Neutrophil adherence to activated saphenous vein and mammary endothelium after graft preparation. Ann. Thorac. Surg. 81, 1262-1268 (2006).
157. Drechsler, M., Doring, Y., Megens, R. T., Soehnlein, O. Neutrophilic granulocytes-promiscuous accelerators of atherosclerosis. Thromb. Haemost. 106, 839-848 (2011).
158. Malinska, A. et al. CD68 expression in aortocoronary saphenous vein bypass grafts. Histochem. Cell Biol. 140, 183-188 (2013).
159. Packard, R. R., Lichtman, A. H., Libby, P. Innate and adaptive immunity in atherosclerosis. Semin. Immunopathol. 31, 5-22 (2009).
160. Ewing, M. M. et al. Annexin A5 therapy attenuates vascular inflammation and remodeling and improves endothelial function in mice. Arterioscler. Thromb. Vasc. Biol. 31, 95-101 (2011).
161. Koga, J. et al. Macrophage Notch ligand Delta-like 4 promotes vein graft lesion development: Implications for the treatment of vein graft failure. Arterioscler. Thromb. Vasc. Biol. 35, 2343-2353 (2015).
162. Cherian, S. M. et al. Immunohistochemical and ultrastructural evidence that dendritic cells infiltrate stenotic aortocoronary saphenous vein bypass grafts. Cardiovasc. Surg. 9, 194-200 (2001).
163. Moore, K. J., Tabas, I. Macrophages in the pathogenesis of atherosclerosis. Cell 145, 341-355 (2011).
164. Ozmen, J., Bobryshev, Y. V., Lord, R. S. CD40 co-stimulatory molecule expression by dendritic cells in primary atherosclerotic lesions in carotid arteries and in stenotic saphenous vein coronary artery grafts. Cardiovasc. Surg. 9, 329-333 (2001).
165. Shi, G. P., Bot, I., Kovanen, P. T. Mast cells in human and experimental cardiometabolic diseases. Nat. Rev. Cardiol. 12, 643-658 (2015).
166. el-Lati, S. G., Dahinden, C. A., Church, M. K. Complement peptides C3a-and C5a-induced mediator release from dissociated human skin mast cells. J. Invest. Dermatol. 102, 803-806 (1994).
167. Cross, K. S. et al. Mast cell infiltration: A possible mechanism for vein graft vasospasm. Surgery 104, 171-177 (1988).
168. Kovanen, P. T. Mast cells and degradation of pericellular and extracellular matrices: Potential contributions to erosion, rupture and intraplaque haemorrhage of atherosclerotic plaques. Biochem. Soc. Trans. 35, 857-861 (2007).
169. Wezel, A., Quax, P. H., Kuiper, J., Bot, I. The role of mast cells in atherosclerosis. Hamostaseologie 35, 113-120 (2015).
170. Schober, A. Chemokines in vascular dysfunction and remodeling. Arterioscler. Thromb. Vasc. Biol. 28, 1950-1959 (2008).
171. de Vries, M. R. et al. C57BL/6 NK cell gene complex is crucially involved in vascular remodeling. J. Mol. Cell. Cardiol. 64, 51-58 (2013).
172. Carpenter, J. P., Tomaszewski, J. E. Human saphenous vein allograft bypass grafts: Immune response. J. Vasc. Surg. 27, 492-499 (1998).
173. Andersson, J., Libby, P., Hansson, G. K. Adaptive immunity and atherosclerosis. Clin. Immunol. 134, 33-46 (2010).
174. Ewing, M. M. et al. T-cell co-stimulation by CD28-CD80/86 and its negative regulator CTLA-4 strongly influence accelerated atherosclerosis development. Int. J. Cardiol. 168, 1965-1974 (2013).
175. Butany, J. W., David, T. E., Ojha, M. Histological and morphometric analyses of early and late aortocoronary vein grafts and distal anastomoses. Can. J. Cardiol. 14, 671-677 (1998).
176. Lu, D. Y. et al. Vein graft adaptation and fistula maturation in the arterial environment. J. Surg. Res. 188, 162-173 (2014).
177. Muto, A., Model, L., Ziegler, K., Eghbalieh, S. D., Dardik, A. Mechanisms of vein graft adaptation to the arterial circulation: Insights into the neointimal algorithm and management strategies. Circ. J. 74, 1501-1512 (2010).
178. Westerband, A. et al. Immunocytochemical determination of cell type and proliferation rate in human vein graft stenoses. J. Vasc. Surg. 25, 64-73 (1997).
179. Moreno, K. et al. Circulating inflammatory cells are associated with vein graft stenosis. J. Vasc. Surg. 54, 1124-1130 (2011).
180. Yazdani, S. K. et al. Pathology of drug-eluting versus bare-metal stents in saphenous vein bypass graft lesions. JACC Cardiovasc. Interv. 5, 666-674 (2012).
181. Wezel, A. et al. Complement factor C5a induces atherosclerotic plaque disruptions. J. Cell. Mol. Med. 18, 2020-2030 (2014).
182. Li, J. et al. The patency of sequential and individual vein coronary bypass grafts: A systematic review. Ann. Thorac. Surg. 92, 1292-1298 (2011).
183. Souza, D. A new no-touch preparation technique. Technical notes. Scand. J. Thorac. Cardiovasc. Surg. 30, 41-44 (1996).
184. Souza, D. S. et al. Improved patency in vein grafts harvested with surrounding tissue: Results of a randomized study using three harvesting techniques. Ann. Thorac. Surg. 73, 1189-1195 (2002).
185. Souza, D. S. et al. Harvesting the saphenous vein with surrounding tissue for CABG provides long-term graft patency comparable to the left internal thoracic artery: Results of a randomized longitudinal trial. J. Thorac. Cardiovasc. Surg. 132, 373-378 (2006).
186. Verma, S. et al. Pedicled no-touch saphenous vein graft harvest limits vascular smooth muscle cell activation: The PATENT saphenous vein graft study. Eur. J. Cardiothorac. Surg. 45, 717-725 (2014).
187. Samano, N. et al. The no-touch saphenous vein for coronary artery bypass grafting maintains a patency, after 16 years, comparable to the left internal thoracic artery: A randomized trial. J. Thorac. Cardiovasc. Surg. 150, 880-888 (2015).
188. US National Library of Science. ClinicalTrials.gov http://clinicaltrials.gov/show/NCT01047449 (2016).
189. Allen, K. et al. Endoscopic vascular harvest in coronary artery bypass grafting surgery: A consensus statement of the International Society of Minimally Invasive Cardiothoracic Surgery (ISMICS) 2005. Innovations (Phila.) 1, 51-60 (2005).
190. Williams, J. B. et al. Association between endoscopic versus open vein-graft harvesting and mortality, wound complications, and cardiovascular events in patients undergoing CABG surgery. JAMA 308, 475-484 (2012).
191. Zenati, M. A. et al. Impact of endoscopic versus open saphenous vein harvest technique on late coronary artery bypass grafting patient outcomes in the ROOBY (Randomized On/Off Bypass) Trial. J. Thorac. Cardiovasc. Surg. 141, 338-344 (2011).
192. van, D. S. et al. Endoscopic harvesting device type and outcomes in patients undergoing coronary artery bypass surgery. Ann. Surg. 260, 402-408 (2014).
193. Teixeira, P. G., Woo, K., Weaver, F. A., Rowe, V. L. Vein harvesting technique for infrainguinal arterial bypass with great saphenous vein and its association with surgical site infection and graft patency. J. Vasc. Surg. 61, 1264-1271 (2015).
194. Grant, S. W. et al. What is the impact of endoscopic vein harvesting on clinical outcomes following coronary artery bypass graft surgery Heart 98, 60-64 (2012).
195. Deppe, A. C. et al. Endoscopic vein harvesting for coronary artery bypass grafting: A systematic review with meta-analysis of 27,789 patients. J. Surg. Res. 180, 114-124 (2013).
196. Zenati, M. A. et al. Choice of vein-harvest technique for coronary artery bypass grafting: Rationale and design of the REGROUP trial. Clin. Cardiol. 37, 325-330 (2014).
197. Wise, E. S. et al. Preservation solution impacts physiologic function and cellular viability of human saphenous vein graft. Surgery 158, 537-546 (2015).
198. Tsakok, M., Montgomery-Taylor, S., Tsakok, T. Storage of saphenous vein grafts prior to coronary artery bypass grafting: Is autologous whole blood more effective than saline in preserving graft function Interact. Cardiovasc. Thorac. Surg. 15, 720-725 (2012).
199. Barber, D. A., Rubin, J. W., Zumbro, G. L., Tackett, R. L. The use of methylene blue as an extravascular surgical marker impairs vascular responses of human saphenous veins. J. Thorac. Cardiovasc. Surg. 109, 21-29 (1995).
200. Hocking, K. M. et al. Brilliant blue FCF is a nontoxic dye for saphenous vein graft marking that abrogates response to injury. J. Vasc. Surg. http:/dx.doi.org/10.1016/j.jvs.2014.12.059 (2015).
201. Conte, M. S. Technical factors in lower-extremity vein bypass surgery: How can we improve outcomes Semin. Vasc. Surg. 22, 227-233 (2009).
202. Sottiurai, V. S. Comparison of reversed, nonreversed translocated, and in situ vein grafts in arterial revascularization: Techniques, cumulative patency, versatility, and durability. Int. J. Angiol. 8, 197-202 (1999).
203. Wengerter, K. R. et al. Prospective randomized multicenter comparison of in situ and reversed vein infrapopliteal bypasses. J. Vasc. Surg. 13, 189-197 (1991).
204. Parang, P., Arora, R. Coronary vein graft disease: Pathogenesis and prevention. Can. J. Cardiol. 25, e57-e62 (2009).
205. Pantely, G. A. et al. Failure of antiplatelet and anticoagulant therapy to improve patency of grafts after coronary-artery bypass: A controlled, randomized study. N. Engl. J. Med. 301, 962-966 (1979).
206. McEnany, M. T. et al. The effect of antithrombotic therapy on patency rates of saphenous vein coronary artery bypass grafts. J. Thorac. Cardiovasc. Surg. 83, 81-89 (1982).
207. Sharma, G. V., Khuri, S. F., Josa, M., Folland, E. D., Parisi, A. F. The effect of antiplatelet therapy on saphenous vein coronary artery bypass graft patency. Circulation 68, II218-II221 (1983).
208. Goldman, S. et al. Saphenous vein graft patency 1 year after coronary artery bypass surgery and effects of antiplatelet therapy. Results of a Veterans Administration Cooperative Study. Circulation 80, 1190-1197 (1989).
209. Chesebro, J. H. et al. Effect of dipyridamole and aspirin on late vein-graft patency after coronary bypass operations. N. Engl. J. Med. 310, 209-214 (1984).
210. Windecker, S. et al. 2014 ESC/EACTS guidelines on myocardial revascularization: The Task Force on Myocardial Revascularization of the European Society of Cardiology (ESC) and the European Association for Cardio-Thoracic Surgery (EACTS). Developed with the special contribution of the European Association of Percutaneous Cardiovascular Interventions (EAPCI). Eur. Heart J. 35, 2541-2619 (2014).
211. Chevigne, M., David, J. L., Rigo, P., Limet, R. Effect of ticlopidine on saphenous vein bypass patency rates: A double-blind study. Ann. Thorac. Surg. 37, 371-378 (1984).
212. Limet, R., David, J. L., Magotteaux, P., Larock, M. P., Rigo, P. Prevention of aorta-coronary bypass graft occlusion. Beneficial effect of ticlopidine on early and late patency rates of venous coronary bypass grafts: A double-blind study. J. Thorac. Cardiovasc. Surg. 94, 773-783 (1987).
213. Becquemin, J. P. Effect of ticlopidine on the long-term patency of saphenous-vein bypass grafts in the legs. Etude de la Ticlopidine après Pontage Fémoro-Poplité and the Association Universitaire de Recherche en Chirurgie. N. Engl. J. Med. 337, 1726-1731 (1997).
214. Quinn, M. J., Fitzgerald, D. J. Ticlopidine and clopidogrel. Circulation 100, 1667-1672 (1999).
215. Shigematsu, H., Komori, K., Tanemoto, K., Harada, Y., Nakamura, M. Clopidogrel for Atherothrombotic Event Management in Patients with Peripheral Arterial Disease (COOPER) Study: Safety and efficacy of clopidogrel versus ticlopidine in Japanese patients. Ann. Vasc. Dis. 5, 364-375 (2012).
216. Belch, J. J. et al. Results of the randomized, placebo-controlled clopidogrel and acetylsalicylic acid in bypass surgery for peripheral arterial disease (CASPAR) trial. J. Vasc. Surg. 52, 825-833.e2 (2010).
217. Deo, S. V. et al. Dual anti-platelet therapy after coronary artery bypass grafting: Is there any benefit A systematic review and meta-analysis. J. Card. Surg. 28, 109-116 (2013).
218. Mujanovic, E. et al. The effect of combined clopidogrel and aspirin therapy after off-pump coronary surgery: A pilot study. Innovations (Phila.) 4, 265-268 (2009).
219. Gao, G. et al. Aspirin plus clopidogrel therapy increases early venous graft patency after coronary artery bypass surgery a single-center, randomized, controlled trial. J. Am. Coll. Cardiol. 56, 1639-1643 (2010).
220. Sun, J. C. et al. Randomized trial of aspirin and clopidogrel versus aspirin alone for the prevention of coronary artery bypass graft occlusion: The Preoperative Aspirin and Postoperative Antiplatelets in Coronary Artery Bypass Grafting study. Am. Heart J. 160, 1178-1184 (2010).
221. van der Meer, J. et al. Prevention of one-year vein-graft occlusion after aortocoronary-bypass surgery: A comparison of low-dose aspirin, low-dose aspirin plus dipyridamole, and oral anticoagulants. The CABADAS Research Group of the Interuniversity Cardiology Institute of The Netherlands. Lancet 342, 257-264 (1993).
222. Fremes, S. E. et al. Optimal antithrombotic therapy following aortocoronary bypass: A meta-analysis. Eur. J. Cardiothorac. Surg. 7, 169-180 (1993).
223. Lim, E. et al. Indirect comparison meta-analysis of aspirin therapy after coronary surgery. BMJ 327, 1309 (2003).
224. Johnson, W. C., Williford, W. O. Benefits, morbidity, and mortality associated with long-term administration of oral anticoagulant therapy to patients with peripheral arterial bypass procedures: A prospective randomized study. J. Vasc. Surg. 35, 413-421 (2002).
225. Bedenis, R., Lethaby, A., Maxwell, H., Acosta, S., Prins, M. H. Antiplatelet agents for preventing thrombosis after peripheral arterial bypass surgery. Cochrane Database Syst. Rev. 2, CD000535 (2015).
226. Lee, J. Y., Sung, K. C., Choi, H. I. Comparison of aspirin and indobufen in healthy volunteers. Platelets 27, 105-109 (2016).
227. D'Addato, M. et al. Indobufen versus acetylsalicylic acid plus dipyridamole in long-term patency after femoropopliteal bypass. Int. Angiol. 11, 106-112 (1992).
228. Rajah, S. M. et al. Effects of antiplatelet therapy with indobufen or aspirin-dipyridamole on graft patency one year after coronary artery bypass grafting. J. Thorac. Cardiovasc. Surg. 107, 1146-1153 (1994).
229. Cataldo, G., Heiman, F., Lavezzari, M., Marubini, E. Indobufen compared with aspirin and dipyridamole on graft patency after coronary artery bypass surgery: Results of a combined analysis. Coron. Artery Dis. 9, 217-222 (1998).
230. Geraghty, A. J., Welch, K. Antithrombotic agents for preventing thrombosis after infrainguinal arterial bypass surgery. Cochrane Database Syst. Rev. 6, CD000536 (2011).
231. Venkatesan, S. et al. Effects of five preoperative cardiovascular drugs on mortality after coronary artery bypass surgery: A retrospective analysis of an observational study of 16,192 patients. Eur. J. Anaesthesiol. 33, 49-57 (2016).
232. Algra, A., Tangelder, M. J., Lawson, J. A., Eikelboom, B. C. Interpretation of Dutch BOA trial. Dutch Bypass Oral anticoagulants or Aspirin study group. Lancet 355, 1186-1187 (2000).
233. Negre-Aminou, P. et al. Inhibition of proliferation of human smooth muscle cells by various HMG-CoA reductase inhibitors; comparison with other human cell types. Biochim. Biophys. Acta 1345, 259-268 (1997).
234. Bustos, C. et al. HMG-CoA reductase inhibition by atorvastatin reduces neointimal inflammation in a rabbit model of atherosclerosis. J. Am. Coll. Cardiol. 32, 2057-2064 (1998).
235. Indolfi, C. et al. Effects of hydroxymethylglutaryl coenzyme A reductase inhibitor simvastatin on smooth muscle cell proliferation in vitro and neointimal formation in vivo after vascular injury. J. Am. Coll. Cardiol. 35, 214-221 (2000).
236. Corpataux, J. M., Naik, J., Porter, K. E., London, N. J. A comparison of six statins on the development of intimal hyperplasia in a human vein culture model. Eur. J. Vasc. Endovasc. Surg. 29, 177-181 (2005).
237. Kulik, A. et al. Impact of statin use on outcomes after coronary artery bypass graft surgery. Circulation 118, 1785-1792 (2008).
238. Jerzewski, K., Ruel, M., Voisine, P., Le May, M. R., Kulik, A. Does high-density lipoprotein influence the development of saphenous vein graft disease after coronary bypass surgery: Exploratory analysis from the CASCADE trial. J. Cardiothorac. Surg. 8, 172 (2013).
239. Spiliopoulos, S., Pastromas, G. Current status of high on-treatment platelet reactivity in patients with coronary or peripheral arterial disease: Mechanisms, evaluation and clinical implications. World J. Cardiol. 7, 912-921 (2015).
240. Hansson, E. C. et al. Coronary artery bypass grafting-related bleeding complications in patients treated with ticagrelor or clopidogrel: A nationwide study. Eur. Heart J. 37, 189-197 (2016).
241. Spiliopoulos, S. et al. Initial experience with ticagrelor in patients with critical limb ischemia and high on-clopidogrel platelet reactivity undergoing complex peripheral endovascular procedures. Cardiovasc. Intervent. Radiol. 37, 1450-1457 (2014).
242. Amico, F., Amico, A., Mazzoni, J., Moshiyakhov, M., Tamparo, W. The evolution of dual antiplatelet therapy in the setting of acute coronary syndrome: Ticagrelor versus clopidogrel. Postgrad. Med. 128, 159-163 (2016).
243. US National Library of Science. ClinicalTrials.gov http://clinicaltrials.gov/show/NCT01755520 (2016).
244. Leonardi, S., Tricoci, P., Becker, R. C. Thrombin receptor antagonists for the treatment of atherothrombosis: Therapeutic potential of vorapaxar and E-5555. Drugs 70, 1771-1783 (2010).
245. de Souza, B. F., Tricoci, P. Novel anti-platelet agents: Focus on thrombin receptor antagonists. J. Cardiovasc. Transl. Res. 6, 415-424 (2013).
246. Becker, R. C. et al. Safety and tolerability of SCH 530348 in patients undergoing non-urgent percutaneous coronary intervention: A randomised, double-blind, placebo-controlled phase II study. Lancet 373, 919-928 (2009).
247. Morrow, D. A. et al. Vorapaxar in the secondary prevention of atherothrombotic events. N. Engl. J. Med. 366, 1404-1413 (2012).
248. Bohula, E. A. et al. Efficacy and safety of vorapaxar with and without a thienopyridine for secondary prevention in patients with previous myocardial infarction and no history of stroke or transient ischemic attack. Circulation 132, 1871-1879 (2015).
249. Whellan, D. J. et al. Vorapaxar in acute coronary syndrome patients undergoing coronary artery bypass graft surgery: Subgroup analysis from the TRACER trial (Thrombin Receptor Antagonist for Clinical Event Reduction in Acute Coronary Syndrome). J. Am. Coll. Cardiol. 63, 1048-1057 (2014).
250. Goto, S., Ogawa, H., Takeuchi, M., Flather, M. D., Bhatt, D. L. Double-blind, placebo-controlled Phase II studies of the protease-activated receptor 1 antagonist E5555 (atopaxar) in Japanese patients with acute coronary syndrome or high-risk coronary artery disease. Eur. Heart J. 31, 2601-2613 (2010).
251. Kogushi, M. et al. Oral administration of the thrombin receptor antagonist E5555 (atopaxar) attenuates intimal thickening following balloon injury in rats. Eur. J. Pharmacol. 666, 158-164 (2011).
252. Conte, M. S. et al. A single nucleotide polymorphism in the p27Kip1 gene is associated with primary patency of lower extremity vein bypass grafts. J. Vasc. Surg. 57, 1179-1185 (2013).
253. O'Donoghue, M. L. et al. Safety and tolerability of atopaxar in the treatment of patients with acute coronary syndromes: The lessons from antagonizing the cellular effects of Thrombin-Acute Coronary Syndromes Trial. Circulation 123, 1843-1853 (2011).
254. Wiviott, S. D. et al. Randomized trial of atopaxar in the treatment of patients with coronary artery disease: The lessons from antagonizing the cellular effect of Thrombin-Coronary Artery Disease Trial. Circulation 123, 1854-1863 (2011).
255. Louis, S. F., Zahradka, P. Vascular smooth muscle cell motility: From migration to invasion. Exp. Clin. Cardiol. 15, e75-e85 (2010).
256. Chung, A. W. et al. Arterialization of a vein graft promotes cell cycle progression through Akt and p38 mitogen-activated protein kinase pathways: Impact of the preparation procedure. Can. J. Cardiol. 23, 1147-1154 (2007).
257. Cheng, J. et al. The mechanical stress-activated serum-, glucocorticoid-regulated kinase 1 contributes to neointima formation in vein grafts. Circ. Res. 107, 1265-1274 (2010).
258. Murphy, G. J. et al. Short-and long-term effects of cytochalasin D, paclitaxel and rapamycin on wall thickening in experimental porcine vein grafts. Cardiovasc. Res. 73, 607-617 (2007).
259. Chen, H. L., Liu, K., Meng, X. Y., Wen, X. D., You, Q. S. Local application of rapamycin inhibits vein graft restenosis in rabbits. Transplant. Proc. 43, 2017-2021 (2011).
260. Rajathurai, T. et al. Periadventitial rapamycin-eluting microbeads promote vein graft disease in long-term pig vein-into-artery interposition grafts. Circ. Cardiovasc. Interv. 3, 157-165 (2010).
261. Ehsan, A., Mann, M. J., Dell'Acqua, G., Dzau, V. J. Long-term stabilization of vein graft wall architecture and prolonged resistance to experimental atherosclerosis after E2F decoy oligonucleotide gene therapy. J. Thorac. Cardiovasc. Surg. 121, 714-722 (2001).
262. Mann, M. J. et al. Ex-vivo gene therapy of human vascular bypass grafts with E2F decoy: The PREVENT single-centre, randomised, controlled trial. Lancet 354, 1493-1498 (1999).
263. Harskamp, R. E. et al. Vein graft preservation solutions, patency, and outcomes after coronary artery bypass graft surgery: Follow-up from the PREVENT IV randomized clinical trial. JAMA Surg. 149, 798-805 (2014).
264. Conte, M. S. et al. Design and rationale of the PREVENT III clinical trial: Edifoligide for the prevention of infrainguinal vein graft failure. Vasc. Endovasc. Surg. 39, 15-23 (2005).
265. Southerland, K. W., Frazier, S. B., Bowles, D. E., Milano, C. A., Kontos, C. D. Gene therapy for the prevention of vein graft disease. Transl. Res. 161, 321-338 (2013).
266. Wang, X. W., Zhao, X. J., Xiang, X. Y. Gene therapy for vein graft failure. J. Card. Surg. 28, 144-147 (2013).
267. Pradhan-Nabzdyk, L., Huang, C., LoGerfo, F. W., Nabzdyk, C. S. Current siRNA targets in the prevention and treatment of intimal hyperplasia. Discov. Med. 18, 125-132 (2014).
268. Taggart, D. P. et al. A randomized trial of external stenting for saphenous vein grafts in coronary artery bypass grafting. Ann. Thorac. Surg. 99, 2039-2045 (2015).
269. Murphy, G. J., Newby, A. C., Jeremy, J. Y., Baumbach, A., Angelini, G. D. A randomized trial of an external Dacron sheath for the prevention of vein graft disease: The Extent study. J. Thorac. Cardiovasc. Surg. 134, 504-505 (2007).
270. Schoettler, J. et al. Highly flexible nitinol mesh to encase aortocoronary saphenous vein grafts: First clinical experiences and angiographic results nine months postoperatively. Interact. Cardiovasc. Thorac. Surg. 13, 396-400 (2011).
271. Emery, R. W., Solien, E., Klima, U. Clinical evaluation of the eSVS Mesh: First-in-Man trial outcomes. ASAIO J. 61, 178-183 (2015).
272. Ferrari, E., von, S. L., Berdajs, D. Improving coronary artery bypass graft durability: Use of the external saphenous vein graft support. Multimed. Man. Cardiothorac. Surg. http://dx.doi.org/10.1093/mmcts/mmv005 (2015).
273. US National Library of Science. ClinicalTrials.gov http://clinicaltrials.gov/show/NCT02072239 (2015).
274. Riahi, M., Vasu, C. M., Tomatis, L. A., Schlosser, R. J., Zimmerman, G. Aneurysm of saphenous vein bypass graft to coronary artery. J. Thorac. Cardiovasc. Surg. 70, 358-359 (1975).
275. Memon, A. Q., Huang, R. I., Marcus, F., Xavier, L., Alpert, J. Saphenous vein graft aneurysm: Case report and review. Cardiol. Rev. 11, 26-34 (2003).
276. Ramirez, F. D. et al. Natural history and management of aortocoronary saphenous vein graft aneurysms: A systematic review of published cases. Circulation 126, 2248-2256 (2012).
277. Berceli, S. A. et al. Surgical and endovascular revision of infrainguinal vein bypass grafts: Analysis of midterm outcomes from the PREVENT III trial. J. Vasc. Surg. 46, 1173-1179 (2007).
278. Sabik, J. F. et al. Is reoperation still a risk factor in coronary artery bypass surgery Ann. Thorac. Surg. 80, 1719-1727 (2005).
279. Yap, C. H. et al. Contemporary results show repeat coronary artery bypass grafting remains a risk factor for operative mortality. Ann. Thorac. Surg. 87, 1386-1391 (2009).
280. Hindnavis, V., Cho, S. H., Goldberg, S. Saphenous vein graft intervention: A review. J. Invasive Cardiol. 24, 64-71 (2012).
281. Eisenberg, J. A. et al. Is balloon angioplasty of peri-anastomotic stenoses of failing peripheral arterial bypasses worthwhile Vasc. Endovascular Surg. 43, 346-351 (2009).
282. Baim, D. S. et al. Randomized trial of a distal embolic protection device during percutaneous intervention of saphenous vein aorto-coronary bypass grafts. Circulation 105, 1285-1290 (2002).
283. Mehta, S. K. et al. Utilization of distal embolic protection in saphenous vein graft interventions (an analysis of 19,546 patients in the American College of Cardiology-National Cardiovascular Data Registry). Am. J. Cardiol. 100, 1114-1118 (2007).
284. Jukema, J. W., Ahmed, T. A., Verschuren, J. J., Quax, P. H. Restenosis after PCI. Part 2: Prevention and therapy. Nat. Rev. Cardiol. 9, 79-90 (2012).
285. Savage, M. P. et al. Stent placement compared with balloon angioplasty for obstructed coronary bypass grafts. N. Engl. J. Med. 337, 740-747 (1997).
286. Liu, Y. et al. Percutaneous coronary intervention strategies and prognosis for graft lesions following coronary artery bypass grafting. Exp. Ther. Med. 9, 1656-1664 (2015).
287. Ali, H., Elbadawy, A., Saleh, M., Hasaballah, A. Balloon angioplasty for revision of failing lower extremity bypass grafts. J. Vasc. Surg. 62, 93-100 (2015).
288. San Norberto, E. M., Taylor, J. H., Carrera, S., Vaquero, C. Percutaneous transluminal angioplasty with drug-eluting balloons for salvage of infrainguinal bypass grafts. J. Endovasc. Ther. 21, 12-21 (2014).
289. Brennan, J. M. et al. Safety and clinical effectiveness of drug-eluting stents for saphenous vein graft intervention in older individuals: Results from the medicare-linked National Cardiovascular Data Registry CathPCI Registry® (2005-2009). Catheter. Cardiovasc. Interv. http://dx.doi.org/10.1002/ccd.25979 (2015).
290. Piola, M. et al. A compact and automated ex vivo vessel culture system for the pulsatile pressure conditioning of human saphenous veins. J. Tissue Eng. Regen. Med. 10, E204-E215 (2016).
291. Salzberg, S. P. et al. Increased neointimal formation after surgical vein grafting in a murine model of type 2 diabetes. Circulation 114, I302-I307 (2006).
292. Monraats, P. S. et al. Genetic inflammatory factors predict restenosis after percutaneous coronary interventions. Circulation 112, 2417-2425 (2005).
293. Tran-Son-Tay, R. et al. An experiment-based model of vein graft remodeling induced by shear stress. Ann. Biomed. Eng. 36, 1083-1091 (2008).
294. Hwang, M. et al. Rule-based model of vein graft remodeling. PLoS ONE 8, e57822 (2013).
295. Webb, C. M., Orion, E., Taggart, D. P., Channon, K. M., Di, M. C. OCT imaging of aorto-coronary vein graft pathology modified by external stenting: 1-year post-surgery. Eur. Heart J. Cardiovasc. Imaging http://dx.doi.org/10.1093/ehjci/jev310 (2015).
296. Boylan, M. J. et al. Surgical treatment of isolated left anterior descending coronary stenosis. Comparison of left internal mammary artery and venous autograft at 18 to 20 years of follow-up. J. Thorac. Cardiovasc. Surg. 107, 657-662 (1994).
297. Sabik, J. F. et al. Influence of patient characteristics and arterial grafts on freedom from coronary reoperation. J. Thorac. Cardiovasc. Surg. 131, 90-98 (2006).
298. Tatoulis, J. et al. Long-term patency of 1108 radial arterial-coronary angiograms over 10 years. Ann. Thorac. Surg. 88, 23-29 (2009).
299. Benedetto, U., Angeloni, E., Refice, S., Sinatra, R. Radial artery versus saphenous vein graft patency: Meta-analysis of randomized controlled trials. J. Thorac. Cardiovasc. Surg. 139, 229-231 (2010).
300. Goldman, S. et al. Radial artery grafts versus saphenous vein grafts in coronary artery bypass surgery: A randomized trial. JAMA 305, 167-174 (2011).
301. Petrovic, I. et al. Radial artery versus saphenous vein graft used as the second conduit for surgical myocardial revascularization: Long-term clinical follow-up. J. Cardiothorac. Surg. 10, 127 (2015).
302. Cooke, J. P., Chen, Z. A compendium on peripheral arterial disease. Circ. Res. 116, 1505-1508 (2015).
303. O'Donnell, M. E., Reid, J. A., Lau, L. L., Hannon, R. J., Lee, B. Optimal management of peripheral arterial disease for the non-specialist. Ulster Med. J. 80, 33-41 (2011).
304. Ibrahim, K. et al. Effect of clopidogrel on midterm graft patency following off-pump coronary revascularization surgery. Heart Surg. Forum 9, E581-E856 (2006).
305. Kulik, A., Chan, V., Ruel, M. Antiplatelet therapy and coronary artery bypass graft surgery: Perioperative safety and efficacy. Expert Opin. Drug Saf. 8, 169-182 (2009).
306. Ebrahimi, R. et al. Effect of clopidogrel use post coronary artery bypass surgery on graft patency. Ann. Thorac. Surg. 97, 15-21 (2014).
307. Gao, C., Ren, C., Li, D., Li, L. Clopidogrel and aspirin versus clopidogrel alone on graft patency after coronary artery bypass grafting. Ann. Thorac. Surg. 88, 59-62 (2009).
308. Mannacio, V. A. et al. Aspirin plus clopidogrel for optimal platelet inhibition following off-pump coronary artery bypass surgery: Results from the CRYSSA (prevention of Coronary arteRY bypaSS occlusion After off-pump procedures) randomised study. Heart 98, 1710-1715 (2012).
309. Kohler, T. R. et al. Effect of aspirin and dipyridamole on the patency of lower extremity bypass grafts. Surgery 96, 462-466 (1984).
310. Satiani, B. A prospective randomized trial of aspirin in femoral popliteal and tibial bypass grafts. Angiology 36, 608-616 (1985).
311. Clyne, C. A., Archer, T. J., Atuhaire, L. K., Chant, A. D., Webster, J. H. Random control trial of a short course of aspirin and dipyridamole (Persantin) for femorodistal grafts. Br. J. Surg. 74, 246-248 (1987).
312. McCollum, C., Alexander, C., Kenchington, G., Franks, P. J., Greenhalgh, R. Antiplatelet drugs in femoropopliteal vein bypasses: A multicenter trial. J. Vasc. Surg. 13, 150-161 (1991).
313. Edmondson, R. A., Cohen, A. T., Das, S. K., Wagner, M. B., Kakkar, V. V. Low-molecular weight heparin versus aspirin and dipyridamole after femoropopliteal bypass grafting. Lancet 344, 914-918 (1994).
314. Monaco, M. et al. Combination therapy with warfarin plus clopidogrel improves outcomes in femoropopliteal bypass surgery patients. J. Vasc. Surg. 56, 96-105 (2012).