Journal of Vascular Surgery
Volume 51, Issue 3 , Pages 736-746 , March 2010

Adaptive changes in autogenous vein grafts for arterial reconstruction: Clinical implications

  • Christopher D. Owens, MD, MSc

      Affiliations

    • Corresponding Author InformationReprint requests: Christopher D. Owens, MD, MSc, University of California San Francisco, Division of Vascular and Endovascular Surgery, 400 Parnassus Avenue, San Francisco, CA 94143

Received 5 July 2009 ,Accepted 24 July 2009.

References 

  1. Rosamond W, Flegal K, Furie K, Go A, Greenlund K, Haase N, et al. Heart disease and stroke statistics–2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 2008;117:e25–e146
  2. Hirsch AT, Criqui MH, Treat-Jacobson D, Regensteiner JG, Creager MA, Olin JW, et al. Peripheral arterial disease detection, awareness, and treatment in primary care. JAMA. 2001;286:1317–1324
  3. Beckman JA, Goldfine AB, Gordon MB, Creager MA. Ascorbate restores endothelium-dependent vasodilation impaired by acute hyperglycemia in humans. Circulation. 2001;103:1618–1623
  4. Conte MS, Mann MJ, Simosa HF, Rhynhart KK, Mulligan RC. Genetic interventions for vein bypass graft disease: a review. J Vasc Surg. 2002;36:1040–1052
  5. Braun-Dullaeus RC, Mann MJ, Dzau VJ. Cell cycle progression: new therapeutic target for vascular proliferative disease. Circulation. 1998;98:82–89
  6. Conte MS, Bandyk DF, Clowes AW, Moneta GL, Seely L, Lorenz TJ, et al. Results of PREVENT III: a multicenter, randomized trial of edifoligide for the prevention of vein graft failure in lower extremity bypass surgery. J Vasc Surg. 2006;43:742–751discussion 751
  7. Kaneda H, Terashima M, Takahashi T, Iversen S, Felderhoff T, Grube E, et al. Mechanisms of lumen narrowing of saphenous vein bypass grafts 12 months after implantation: an intravascular ultrasound study. Am Heart J. 2006;151:726–729
  8. Mitsouras D, Mulkern RV, Owens CD, Conte MS, Ersoy H, Luu TM, et al. High-resolution peripheral vein bypass graft wall studies using high sampling efficiency inner volume 3D FSE. Magn Reson Med. 2008;59:650–654
  9. Rybicki FJ, Mitsouras D, Owens CD, Whitmore AG, Ersoy H, Mulkern RV, et al. Lower extremity peripheral vein bypass graft wall thickness changes demonstrated at 1 and 6 months after surgery with ultra-high spatial resolution black blood inner volume three-dimensional fast spin echo magnetic resonance imaging. Int J Cardiovasc Imaging. 2008;24:529–533
  10. Owens CD, Wake N, Jacot JG, Gerhard-Herman M, Gaccione P, Belkin M, et al. Early biomechanical changes in lower extremity vein grafts--distinct temporal phases of remodeling and wall stiffness. J Vasc Surg. 2006;44:740–746
  11. Cox JL, Chiasson DA, Gotlieb AI. Stranger in a strange land: the pathogenesis of saphenous vein graft stenosis with emphasis on structural and functional differences between veins and arteries. Prog Cardiovasc Dis. 1991;34:45–68
  12. Milroy CM, Scott DJ, Beard JD, Horrocks M, Bradfield JW. Histological appearances of the long saphenous vein. J Pathol. 1989;159:311–316
  13. Canham PB, Finlay HM, Boughner DR. Contrasting structure of the saphenous vein and internal mammary artery used as coronary bypass vessels. Cardiovasc Res. 1997;34:557–567
  14. Davies AH, Magee TR, Baird RN, Sheffield E, Horrocks M. Vein compliance: a preoperative indicator of vein morphology and of veins at risk of vascular graft stenosis. Br J Surg. 1992;79:1019–1021
  15. Mills JL, Fujitani RM, Taylor SM. The characteristics and anatomic distribution of lesions that cause reversed vein graft failure: a five-year prospective study. J Vasc Surg. 1993;17:195–204discussion 204-6
  16. Davies MG, Hagen PO. Pathophysiology of vein graft failure: a review. Eur J Vasc Endovasc Surg. 1995;9:7–18
  17. Shi Y, O'Brien JE, Mannion JD, Morrison RC, Chung W, Fard A, et al. Remodeling of autologous saphenous vein grafts (The role of perivascular myofibroblasts). Circulation. 1997;95:2684–2693
  18. Shi Y, O'Brien JE, Ala-Kokko L, Chung W, Mannion JD, Zalewski A. Origin of extracellular matrix synthesis during coronary repair. Circulation. 1997;95:997–1006
  19. Sartore S, Chiavegato A, Faggin E, Franch R, Puato M, Ausoni S, et al. Contribution of adventitial fibroblasts to neointima formation and vascular remodeling: from innocent bystander to active participant. Circ Res. 2001;89:1111–1121
  20. Zalewski A, Shi Y, Johnson AG. Diverse origin of intimal cells: smooth muscle cells, myofibroblasts, fibroblasts, and beyond?. Circ Res. 2002;91:652–655
  21. Zhang L, Freedman NJ, Brian L, Peppel K. Graft-extrinsic cells predominate in vein graft arterialization. Arterioscler Thromb Vasc Biol. 2004;24:470–476
  22. Kalra M, Miller VM. 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. 2000;37:576–584
  23. Ahanchi SS, Tsihlis ND, Kibbe MR. The role of nitric oxide in the pathophysiology of intimal hyperplasia. J Vasc Surg. 2007;45(Suppl A):A64–A73
  24. Davies MG, Klyachkin ML, Dalen H, Massey MF, Svendsen E, Hagen PO. The integrity of experimental vein graft endothelium–implications on the etiology of early graft failure. Eur J Vasc Surg. 1993;7:156–165
  25. Bratt J, Palmblad J. Cytokine-induced neutrophil-mediated injury of human endothelial cells. J Immunol. 1997;159:912–918
  26. Carlos TM, Harlan JM. Leukocyte-endothelial adhesion molecules. Blood. 1994;84:2068–2101
  27. Eslami MH, Gangadharan SP, Belkin M, Donaldson MC, Whittemore AD, Conte MS. Monocyte adhesion to human vein grafts: a marker for occult intraoperative injury?. J Vasc Surg. 2001;34:923–929
  28. Gangadharan SP, Eslami MH, Weiss IP, Sui X, Conte MS. Monocyte adhesion to balloon-injured arteries: the influence of endothelial cell seeding. J Vasc Surg. 2001;33:1247–1254
  29. Chesebro JH, Clements IP, Fuster V, Elveback LR, Smith HC, Bardsley WT, et al. A platelet-inhibitor-drug trial in coronary-artery bypass operations: benefit of perioperative dipyridamole and aspirin therapy on early postoperative vein-graft patency. N Engl J Med. 1982;307:73–78
  30. Chesebro JH, Fuster V, Elveback LR, Clements IP, Smith HC, Holmes DR, et al. Effect of dipyridamole and aspirin on late vein-graft patency after coronary bypass operations. N Engl J Med. 1984;310:209–214
  31. Tsui JC, Souza DS, Filbey D, Karlsson MG, Dashwood MR. Localization of nitric oxide synthase in saphenous vein grafts harvested with a novel “no-touch” technique: potential role of nitric oxide contribution to improved early graft patency rates. J Vasc Surg. 2002;35:356–362
  32. Quist WC, LoGerfo FW. Prevention of smooth muscle cell phenotypic modulation in vein grafts: a histomorphometric study. J Vasc Surg. 1992;16:225–231
  33. Hinokiyama K, Valen G, Tokuno S, Vedin JB, Vaage J. Vein graft harvesting induces inflammation and impairs vessel reactivity. Ann Thorac Surg. 2006;82:1458–1464
  34. Odashiro T, Komori K, Ishii T, Okadome K, Sugimachi K. Comparison of endothelial function between in situ and reversed vein graft: differences in endothelium-dependent responses. Surgery. 1995;117:179–188
  35. Bandyk DF, Schmitt DD, Seabrook GR, Adams MB, Towne JB. Monitoring functional patency of in situ saphenous vein bypasses: the impact of a surveillance protocol and elective revision. J Vasc Surg. 1989;9:286–296
  36. Leather RP, Shah DM, Chang BB, Kaufman JL. Resurrection of the in situ saphenous vein bypass (1000 cases later). Ann Surg. 1988;208:435–442
  37. Fogle MA, Whittemore AD, Couch NP, Mannick JA. A comparison of in situ and reversed saphenous vein grafts for infrainguinal reconstruction. J Vasc Surg. 1987;5:46–52
  38. Haudenschild C, Gould KE, Quist WC, LoGerfo FW. Protection of endothelium in vessel segments excised for grafting. Circulation. 1981;64(2 Pt 2):II101–II107
  39. Davies MG, Hagen PO. Influence of perioperative storage solutions on long-term vein graft function and morphology. Ann Vasc Surg. 1994;8:150–157
  40. Brody WR, Angeli WW, Kosek JC. Histologic fate of the venous coronary artery bypass in dogs. Am J Pathol. 1972;66:111–130
  41. Davies MG, Klyachkin ML, Dalen H, Svendsen E, Hagen PO. Regression of intimal hyperplasia with restoration of endothelium-dependent relaxing factor-mediated relaxation in experimental vein grafts. Surgery. 1993;114:258–270discussion 270-1
  42. Fann JI, Sokoloff MH, Sarris GE, Yun KL, Kosek JC, Miller DC. The reversibility of canine vein-graft arterialization. Circulation. 1990;82(5 Suppl):IV9–IV18
  43. Sterpetti AV, Cucina A, Lepidi S, Randone B, Stipa F, Aromatario C, 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. 1996;23:568–575
  44. Davies MG, Fulton GJ, Svendsen E, Hagen PO. Time course of the regression of intimal hyperplasia in experimental vein grafts. Cardiovasc Pathol. 1999;8:161–168
  45. Morinaga K, Eguchi H, Miyazaki T, Okadome K, Sugimachi K. Development and regression of intimal thickening of arterially transplanted autologous vein grafts in dogs. J Vasc Surg. 1987;5:719–730
  46. Morinaga K, Okadome K, Kuroki M, Miyazaki T, Muto Y, Inokuchi K. Effect of wall shear stress on intimal thickening of arterially transplanted autogenous veins in dogs. J Vasc Surg. 1985;2:430–433
  47. Cambria RA, Lowell RC, Gloviczki P, Miller VM. Chronic changes in blood flow alter endothelium-dependent responses in autogenous vein grafts in dogs. J Vasc Surg. 1994;20:765–773
  48. Galt SW, Zwolak RM, Wagner RJ, Gilbertson JJ. Differential response of arteries and vein grafts to blood flow reduction. J Vasc Surg. 1993;17:563–570
  49. Kohler TR, Kirkman TR, Kraiss LW, Zierler BK, Clowes AW. Increased blood flow inhibits neointimal hyperplasia in endothelialized vascular grafts. Circ Res. 1991;69:1557–1565
  50. Kraiss LW, Kirkman TR, Kohler TR, Zierler B, Clowes AW. Shear stress regulates smooth muscle proliferation and neointimal thickening in porous polytetrafluoroethylene grafts. Arterioscler Thromb. 1991;11:1844–1852
  51. Meyerson SL, Skelly CL, Curi MA, Shakur UM, Vosicky JE, Glagov S, et al. The effects of extremely low shear stress on cellular proliferation and neointimal thickening in the failing bypass graft. J Vasc Surg. 2001;34:90–97
  52. Geary RL, Kohler TR, Vergel S, Kirkman TR, Clowes AW. Time course of flow-induced smooth muscle cell proliferation and intimal thickening in endothelialized baboon vascular grafts. Circ Res. 1994;74:14–23
  53. Dobrin PB, Littooy FN, Endean ED. Mechanical factors predisposing to intimal hyperplasia and medial thickening in autogenous vein grafts. Surgery. 1989;105:393–400
  54. Dimmeler S, Assmus B, Hermann C, Haendeler J, Zeiher AM. Fluid shear stress stimulates phosphorylation of Akt in human endothelial cells: involvement in suppression of apoptosis. Circ Res. 1998;83:334–341
  55. Fisslthaler B, Dimmeler S, Hermann C, Busse R, Fleming I. Phosphorylation and activation of the endothelial nitric oxide synthase by fluid shear stress. Acta Physiol Scand. 2000;168:81–88
  56. Zwolak RM, Adams MC, Clowes AW. Kinetics of vein graft hyperplasia: association with tangential stress. J Vasc Surg. 1987;5:126–136
  57. Tran-Son-Tay R, Hwang M, Garbey M, Jiang Z, Ozaki CK, Berceli SA. An experiment-based model of vein graft remodeling induced by shear stress. Ann Biomed Eng. 2008;36:1083–1091
  58. Tran-Son-Tay R, Hwang M, Berceli SA, Ozaki CK, Garbey M. A model of vein graft intimal hyperplasia. Conf Proc IEEE Eng Med Biol Soc. 2007;2007:5807–5810
  59. Wong AP, Nili N, Jackson ZS, Qiang B, Leong-Poi H, Jaffe R, et al. Expansive remodeling in venous bypass grafts: novel implications for vein graft disease. Atherosclerosis. 2008;196:580–589
  60. Ge J, Liu F, Bhate R, Haude M, Görge G, Baumgart D, et al. Does remodeling occur in the diseased human saphenous vein bypass grafts? (An intravascular ultrasound study). Int J Card Imaging. 1999;15:295–300
  61. Nishioka T, Luo H, Berglund H, Eigler NL, Kim CJ, Tabak SW, et al. Absence of focal compensatory enlargement or constriction in diseased human coronary saphenous vein bypass grafts (An intravascular ultrasound study). Circulation. 1996;93:683–690
  62. Gibbons GH, Dzau VJ. The emerging concept of vascular remodeling. N Engl J Med. 1994;330:1431–1438
  63. O'Brien JE, Ormont ML, Shi Y, Wang D, Zalewski A, Mannion JD. Early injury to the media after saphenous vein grafting. Ann Thorac Surg. 1998;65:1273–1278
  64. Hong MK, Mintz GS, Hong MK, Abizaid AS, Pichard AD, Satler LF, et al. Intravascular ultrasound assessment of the presence of vascular remodeling in diseased human saphenous vein bypass grafts. Am J Cardiol. 1999;84:992–998
  65. Caños DA, Mintz GS, Berzingi CO, Apple S, Kotani J, Pichard AD, et al. Clinical, angiographic, and intravascular ultrasound characteristics of early saphenous vein graft failure. J Am Coll Cardiol. 2004;44:53–56
  66. Mendelsohn FO, Foster GP, Palacios IF, Weyman AE, Weissman NJ. In vivo assessment by intravascular ultrasound of enlargement in saphenous vein bypass grafts. Am J Cardiol. 1995;76:1066–1069
  67. Leotta DF, Primozich JF, Beach KW, Bergelin RO, Zierler RE, Strandness DE. Remodeling in peripheral vein graft revisions: serial study with three-dimensional ultrasound imaging. J Vasc Surg. 2003;37:798–807
  68. Owens CD, Ho KJ, Conte MS. Lower extremity vein graft failure: a translational approach. Vasc Med. 2008;13:63–74
  69. Rodbard S. Vascular caliber. Cardiology. 1975;60:4–49
  70. Murray CD. The physiological principle of minimum work: I. The vascular system and the cost of blood volume. Proc Natl Acad Sci U S A. 1926;12:207–214
  71. Vita JA, Holbrook M, Palmisano J, Shenouda SM, Chung WB, Hamburg NM, et al. Flow-induced arterial remodeling relates to endothelial function in the human forearm. Circulation. 2008;117:3126–3133
  72. Zarins CK, Zatina MA, Giddens DP, Ku DN, Glagov S. Shear stress regulation of artery lumen diameter in experimental atherogenesis. J Vasc Surg. 1987;5:413–420
  73. Glagov S, Weisenberg E, Zarins CK, Stankunavicius R, Kolettis GJ. Compensatory enlargement of human atherosclerotic coronary arteries. N Engl J Med. 1987;316:1371–1375
  74. Back MR, Maynard M, Winkler A, Bandyk DF. Expected flow parameters within hemodialysis access and selection for remedial intervention of nonmaturing conduits. Vasc Endovascular Surg. 2008;42:150–158
  75. Post MJ, Borst C, Kuntz RE. The relative importance of arterial remodeling compared with intimal hyperplasia in lumen renarrowing after balloon angioplasty (A study in the normal rabbit and the hypercholesterolemic Yucatan micropig). Circulation. 1994;89:2816–2821
  76. Skelly CL, Meyerson SL, Curi MA, Loth F, Schwartz LB. The hemodynamics of vein grafts: measurement and meaning. Ann Vasc Surg. 2001;15:110–122
  77. Buga GM, Gold ME, Fukuto JM, Ignarro LJ. Shear stress-induced release of nitric oxide from endothelial cells grown on beads. Hypertension. 1991;17:187–193
  78. Frangos JA, Eskin SG, McIntire LV, Ives CL. Flow effects on prostacyclin production by cultured human endothelial cells. Science. 1985;227:1477–1479
  79. Garanich JS, Pahakis M, Tarbell JM. Shear stress inhibits smooth muscle cell migration via nitric oxide-mediated downregulation of matrix metalloproteinase-2 activity. Am J Physiol Heart Circ Physiol. 2005;288:H2244–H2252
  80. Kubes P, Suzuki M, Granger DN. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci U S A. 1991;88:4651–4655
  81. Kuchan MJ, Frangos JA. Shear stress regulates endothelin-1 release via protein kinase C and cGMP in cultured endothelial cells. Am J Physiol. 1993;264(1 Pt 2):H150–H156
  82. Furchgott RF, Zawadzki JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature. 1980;288:373–376
  83. Stanley JC, Ernst CB, Fry WJ. Fate of 100 aortorenal vein grafts: characteristics of late graft expansion, aneurysmal dilatation, and stenosis. Surgery. 1973;74:931–944
  84. Upchurch GR, Gerhard-Herman MD, Sebastian MW, Belkin M, Conte MS, Donaldson MC, et al. Improved graft patency and altered remodeling in infrainguinal vein graft reconstruction for aneurysmal vs occlusive disease. J Vasc Surg. 1999;29:1022–1030
  85. Dean RH, Wilson JP, Burko H, Foster JH. Saphenous vein aortorenal bypass grafts: serial arteriographic study. Ann Surg. 1974;180:469–478
  86. Szilagyi DE, Smith RF, Elliott JP. Venous autografts in femoropopliteal arterioplasty (Observations in the treatment of occlusive disease). Arch Surg. 1964;89:113–125
  87. Fillinger MF, Cronenwett JL, Besso S, Walsh DB, Zwolak RM. Vein adaptation to the hemodynamic environment of infrainguinal grafts. J Vasc Surg. 1994;19:970–978discussion 978-9
  88. Idu MM, Buth J, Hop WC, Cuypers P, van de Pavoordt ED, Tordoir JM. Factors influencing the development of vein-graft stenosis and their significance for clinical management. Eur J Vasc Endovasc Surg. 1999;17:15–21
  89. Schanzer A, Hevelone N, Owens CD, Belkin M, Bandyk DF, Clowes AW, et al. Technical factors affecting autogenous vein graft failure: observations from a large multicenter trial. J Vasc Surg. 2007;46:1180–1190discussion 1190
  90. Cohen RA, Vanhoutte PM. Endothelium-dependent hyperpolarization (Beyond nitric oxide and cyclic GMP). Circulation. 1995;92:3337–3349
  91. Ozaki CK. Cytokines and the early vein graft: strategies to enhance durability. J Vasc Surg. 2007;45(Suppl A):A92–A98
  92. Owens CD, Ridker PM, Belkin M, Hamdan AD, Pomposelli F, Logerfo F, et al. Elevated C-reactive protein levels are associated with postoperative events in patients undergoing lower extremity vein bypass surgery. J Vasc Surg. 2007;45:2–9discussion 9
  93. Owens CD, Rybicki FJ, Wake N, Schanzer A, Mitsouras D, Gerhard-Herman MD, et al. Early remodeling of lower extremity vein grafts: inflammation influences biomechanical adaptation. J Vasc Surg. 2008;47:1235–1242
  94. Fortmann SP, Ford E, Criqui MH, Folsom AR, Harris TB, Hong Y, et al. CDC/AHA Workshop on markers of inflammation and cardiovascular disease: application to clinical and public health practice: report from the population science discussion group. Circulation. 2004;110:e554–e559
  95. Brevetti G, Silvestro A, Di Giacomo S, Bucur R, Di Donato A, Schiano V, et al. Endothelial dysfunction in peripheral arterial disease is related to increase in plasma markers of inflammation and severity of peripheral circulatory impairment but not to classic risk factors and atherosclerotic burden. J Vasc Surg. 2003;38:374–379
  96. Fichtlscherer S, Rosenberger G, Walter DH, Breuer S, Dimmeler S, Zeiher AM. Elevated C-reactive protein levels and impaired endothelial vasoreactivity in patients with coronary artery disease. Circulation. 2000;102:1000–1006
  97. Brevetti G, Silvestro A, Schiano V, Chiariello M. Endothelial dysfunction and cardiovascular risk prediction in peripheral arterial disease: additive value of flow-mediated dilation to ankle-brachial pressure index. Circulation. 2003;108:2093–2098
  98. Gokce N, Keaney JF, Hunter LM, Watkins MT, Nedeljkovic ZS, Menzoian JO, et al. Predictive value of noninvasively determined endothelial dysfunction for long-term cardiovascular events in patients with peripheral vascular disease. J Am Coll Cardiol. 2003;41:1769–1775
  99. Gokce N, Keaney JF, Hunter LM, Watkins MT, Menzoian JO, Vita JA. Risk stratification for postoperative cardiovascular events via noninvasive assessment of endothelial function: a prospective study. Circulation. 2002;105:1567–1572
  100. Seidel CL, LaRochelle J. Venous and arterial endothelia: different dilator abilities in dog vessels. Circ Res. 1987;60:626–630
  101. Ignarro LJ, Buga GM, Chaudhuri G. EDRF generation and release from perfused bovine pulmonary artery and vein. Eur J Pharmacol. 1988;149:79–88
  102. Vanhoutte PM, Miller VM. Heterogeneity of endothelium-dependent responses in mammalian blood vessels. J Cardiovasc Pharmacol. 1985;7(Suppl 3):S12–S23
  103. Rubanyi GM, Vanhoutte PM. Heterogeneity of endothelium-dependent responses to acetylcholine in canine femoral arteries and veins (Separation of the role played by endothelial and smooth muscle cells). Blood Vessels. 1988;25:75–81
  104. De Mey JG, Vanhoutte PM. Heterogeneous behavior of the canine arterial and venous wall (Importance of the endothelium). Circ Res. 1982;51:439–447
  105. Lüscher TF, Diederich D, Siebenmann R, Lehmann K, Stulz P, von Segesser L, et al. Difference between endothelium-dependent relaxation in arterial and in venous coronary bypass grafts. N Engl J Med. 1988;319:462–467
  106. Schwartz LB, Radic ZS, O'Donohoe MK, Mikat EM, McCann RL, Hagen PO. Saphenous vein endothelium-dependent relaxation in patients with peripheral vascular disease. Ann Vasc Surg. 1992;6:425–432
  107. Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci U S A. 1987;84:9265–9269
  108. Cross KS, Davies MG, el-Sanadiki MN, Murray JJ, Mikat EM, Hagen PO. Long-term human vein graft contractility and morphology: a functional and histopathological study of retrieved coronary vein grafts. Br J Surg. 1994;81:699–705
  109. Park TC, Harker CT, Edwards JM, Moneta GL, Taylor LM, Porter JM. Human saphenous vein grafts explanted from the arterial circulation demonstrate altered smooth-muscle and endothelial responses. J Vasc Surg. 1993;18:61–68discussion 68-9
  110. Ku DD, Caulfield JB, Kirklin JK. Endothelium-dependent responses in long-term human coronary artery bypass grafts. Circulation. 1991;83:402–411
  111. Davies MG, Berkowitz DE, Hagen PO. Constitutive nitric oxide synthase is expressed and nitric oxide-mediated relaxation is preserved in retrieved human aortocoronary vein grafts. J Surg Res. 1995;58:732–738
  112. Chien S. Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. Am J Physiol Heart Circ Physiol. 2007;292:H1209–H1224
  113. Dashwood MR, Savage K, Dooley A, Shi-Wen X, Abraham DJ, Souza DS. Effect of vein graft harvesting on endothelial nitric oxide synthase and nitric oxide production. Ann Thorac Surg. 2005;80:939–944
  114. Sasaki Y, Suehiro S, Becker AE, Kinoshita H, Ueda M. Role of endothelial cell denudation and smooth muscle cell dedifferentiation in neointimal formation of human vein grafts after coronary artery bypass grafting: therapeutic implications. Heart. 2000;83:69–75
  115. Palumbo R, Gaetano C, Melillo G, Toschi E, Remuzzi A, Capogrossi MC. Shear stress downregulation of platelet-derived growth factor receptor-beta and matrix metalloprotease-2 is associated with inhibition of smooth muscle cell invasion and migration. Circulation. 2000;102:225–230
  116. Langille BL, O'Donnell F. Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. Science. 1986;231:405–407
  117. Rizvi MA, Myers PR. Nitric oxide modulates basal and endothelin-induced coronary artery vascular smooth muscle cell proliferation and collagen levels. J Mol Cell Cardiol. 1997;29:1779–1789
  118. 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
  119. Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, et al. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol. 2002;39:257–265
  120. Owens CD, Whitmore A, Mitsourus D, Kim JM, Rybicki F, Conte MS. Radial wall stress is the primary biomechanical force determining wall thickness in human lower extremity vein grafts: assessment of wall characteristics and remodeling patterns using ultra-high resolution magnetic resonance imaging (MRI). In: 2008;Society for Vascular Surgery Vascular Annual Meeting, San Diego, Calif
  121. Wolinsky H, Glagov S. A lamellar unit of aortic medial structure and function in mammals. Circ Res. 1967;20:99–111
  122. Jacot JG, Abdullah I, Belkin M, Gerhard-Herman M, Gaccione P, Polak JF, et al. Early adaptation of human lower extremity vein grafts: wall stiffness changes accompany geometric remodeling. J Vasc Surg. 2004;39:547–555
  123. Hutter MM, Lancaster RT, Henderson WG, Khuri SF, Mosca C, Johnson RG, et al. Comparison of risk-adjusted 30-day postoperative mortality and morbidity in Department of Veterans Affairs hospitals and selected university medical centers: vascular surgical operations in men. J Am Coll Surg. 2007;204:1115–1126
  124. Adam DJ, Beard JD, Cleveland T, Bell J, Bradbury AW, Forbes JF, et al. Bypass versus angioplasty in severe ischaemia of the leg (BASIL): multicentre, randomised controlled trial. Lancet. 2005;366:1925–1934
  125. Nguyen LL, Hevelone N, Rogers SO, Bandyk DF, Clowes AW, Moneta GL, et al. Disparity in outcomes of surgical revascularization for limb salvage: race and gender are synergistic determinants of vein graft failure and limb loss. Circulation. 2009;119:123–130
  126. Nguyen LL, Brahmanandam S, Bandyk DF, Belkin M, Clowes AW, Moneta GL, et al. Female gender and oral anticoagulants are associated with wound complications in lower extremity vein bypass: an analysis of 1404 operations for critical limb ischemia. J Vasc Surg. 2007;46:1191–1197
  127. Nguyen LL, Moneta GL, Conte MS, Bandyk DF, Clowes AW, Seely BL PREVENT III Investigators. Prospective multicenter study of quality of life before and after lower extremity vein bypass in 1404 patients with critical limb ischemia. J Vasc Surg. 2006;44:977–983discussion 983-4
  128. Nguyen LL, Lipsitz SR, Bandyk DF, Clowes AW, Moneta GL, Belkin M, et al. Resource utilization in the treatment of critical limb ischemia: the effect of tissue loss, comorbidities, and graft-related events. J Vasc Surg. 2006;44:971–975discussion 975-6
  129. Berceli SA, Hevelone ND, Lipsitz SR, Bandyk DF, Clowes AW, Moneta GL, et al. Surgical and endovascular revision of infrainguinal vein bypass grafts: analysis of midterm outcomes from the PREVENT III trial. J Vasc Surg. 2007;46:1173–1179
  130. Schanzer A, Hevelone N, Owens CD, Beckman JA, Belkin M, Conte MS. Statins are independently associated with reduced mortality in patients undergoing infrainguinal bypass graft surgery for critical limb ischemia. J Vasc Surg. 2008;47:774–781
  131. Schanzer A, Mega J, Meadows J, Samson RH, Bandyk DF, Conte MS. Risk stratification in critical limb ischemia: derivation and validation of a model to predict amputation-free survival using multicenter surgical outcomes data. J Vasc Surg. 2008;48:1464–1471
  132. Conte MS, Bandyk DF, Clowes AW, Moneta GL, Namini H, Seely L. Risk factors, medical therapies and perioperative events in limb salvage surgery: observations from the PREVENT III multicenter trial. J Vasc Surg. 2005;42:456–464discussion 464-5
  133. Bradbury AW. Long-term (5-year) results of BASIL trial show “open surgery first” to be superior to “endovascular treatment first” for critical limb ischemia. http://www.veithsymposium.org/pdf/aim/1579.pdf2008;cited 2009 June 27
  134. Kalinowski L, Dobrucki IT, Malinski T. Race-specific differences in endothelial function: predisposition of African Americans to vascular diseases. Circulation. 2004;109:2511–2517
  135. Grubbs AL, Anstadt MP, Ergul A. Saphenous vein endothelin system expression and activity in African American patients. Arterioscler Thromb Vasc Biol. 2002;22:1122–1127
  136. Albert MA, Ridker PM. Inflammatory biomarkers in African Americans: a potential link to accelerated atherosclerosis. Rev Cardiovasc Med. 2004;5(Suppl 3):S22–S27
  137. Khera A, McGuire DK, Murphy SA, Stanek HG, Das SR, Vongpatanasin W, et al. Race and gender differences in C-reactive protein levels. J Am Coll Cardiol. 2005;46:464–469
  138. Geary RL, Nikkari ST, Wagner WD, Williams JK, Adams MR, Dean RH. Wound healing: a paradigm for lumen narrowing after arterial reconstruction. J Vasc Surg. 1998;27:96–106discussion 106-8
  139. Conte MS, Belkin M, Upchurch GR, Mannick JA, Whittemore AD, Donaldson MC. Impact of increasing comorbidity on infrainguinal reconstruction: a 20-year perspective. Ann Surg. 2001;233:445–452

 Competition of interest: none.

 The study was funded by the National Heart, Lung, and Blood Institute R01, HL75771, K23 HL 92163, and the American Vascular Association.

 The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a competition of interest.

PII: S0741-5214(09)01574-2

doi: 10.1016/j.jvs.2009.07.102

Journal of Vascular Surgery
Volume 51, Issue 3 , Pages 736-746 , March 2010

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