Vein graft failure

Last updated

In medicine, vein graft failure (VGF) is a condition in which vein grafts, which are used as alternative conduits in bypass surgeries (e.g. CABG), get occluded.

Contents

Veins, mainly the great saphenous vein (GSV) are the most frequently used conduits in bypass surgeries (CABG or PABG), due to their ease of use and availability. [1] Some structural changes of intima thickening and vein wall remodeling are necessary for vein graft adaptation to the arterial environment. The reasons why some of the grafts progress to clinical stenosis is unknown. The patency rates of saphenous vein grafts after CABG at 1 year is approximately 80%. [2] [3] After 5 years the patency rate drops to 65% and at 10 years GSV patency rates are approximately 50%, with only half of the veins are atherosclerosis free. [4] VGF may be identified in asymptomatic patients, but can also produce symptoms of ischemia, depending on the area of the supplied territory of the heart, and the function of native arteries and other grafts. VGF has been closely correlated with revascularization, myocardial infarction and death. [2] [5] Treatment of occluded GSVs can be performed by percutaneous coronary intervention or redo CABG and is considered to be challenging, and thus preventing their obstruction is of great importance. [6]

Mechanism

During and after the harvesting, veins go through a period of ischemia and reperfusion after engraftment, which causes damage to endothelial and smooth muscle cells (SMC). [7] The grafting exposes the vein to arterial pressure and flow that causes increased shear stress and wall tension, which further damages the endothelial layer and SMC. [8] The damage causes local release of tissue factors and reduced bioavailability of prostacyclin and nitric oxide (NO), all of which contribute to platelet activation, deposition of fibrin, which promotes thrombosis. [9] Growth factors that released from macrophages and platelets lead to increased proliferation and migration of SMCs to the intima. The migrated SMC release extracellular matrix resulting in reduced intimal cellularity. [10] Low levels of endothelial nitric oxide, adenosine and prostaglandins, further contribute to SMC proliferation. [11] [12] [13] Over time continued SMC migration and proliferation cause extracellular matrix deposition and fibrotic change that lead to development of intimal hyperplasia, which results in luminal loss that makes the graft more susceptible to atherosclerosis. [14] Progressive atherosclerosis is the primarily cause of late vein graft failure. Vein graft atherosclerotic lesions are more diffuse and concentric, yet less calcified, compared to native atherosclerotic lesions, and are more susceptible to thrombosis formation and rupture. [15]

Graft failure depending on saphenous vein harvesting technique

Having an intact outer fat pedicle is what differentiates the two main techniques for harvesting saphenous vein grafts. Conventionally, the outer fat pedicle is removed during the harvesting process. It has been proposed that the no-touch technique, leaving the outer fat pedicle intact, will cause less endothelial damage at the time of harvest. [16] This lessens intimal hyperplasia in the long run. [17]

Prevention

Statins and antiplatelets such as aspirin, are the only medications recommended by the ESC guidelines and the ACC/AHA Task Force guidelines for the prevention of VGF. [18] [19] [20] [21] Different surgical techniques had been studied in attempt to reduce VGF. The No-touch technique is where the vein is harvested with the surrounding tissues, keeping the vasa vasorum and the nerves in the adventitia intact. This technique shown to improve vein graft patency and less development of intimal hyperplasia. [22] [23] Despite the benefits shown, the use of No-touch technique in CABG is limited to a few centers. Probably because of the shift toward improved cosmetic outcome and patient satisfaction provided by endoscopic vein harvesting (EVH). [24] Although, EVH has been associated with higher risk of vein graft stenosis and occlusion. [25] The solutions in which vein grafts are stored after harvesting also play an important role. Buffered saline, instead of saline or blood, has shown to reduce the risk of significant stenosis or occlusion. [26] Providing the vein with external support prior to grafting has shown to reduce intimal hyperplasia formation and improve the hemodynamics within the graft. [27] [28] [29] Gene therapy is another strategy that been suggested to prevent VGF as the veins are ideally suited for ex vivo treatment prior to grafting. Preclinical studies showed that such strategy has the potential to reduce intimal hyperplasia but more clinical data is needed. [30] [31] [32] [33]

Related Research Articles

<span class="mw-page-title-main">Angioplasty</span> Procedure to widen narrow arteries or veins

Angioplasty, also known as balloon angioplasty and percutaneous transluminal angioplasty (PTA), is a minimally invasive endovascular procedure used to widen narrowed or obstructed arteries or veins, typically to treat arterial atherosclerosis. A deflated balloon attached to a catheter is passed over a guide-wire into the narrowed vessel and then inflated to a fixed size. The balloon forces expansion of the blood vessel and the surrounding muscular wall, allowing an improved blood flow. A stent may be inserted at the time of ballooning to ensure the vessel remains open, and the balloon is then deflated and withdrawn. Angioplasty has come to include all manner of vascular interventions that are typically performed percutaneously.

<span class="mw-page-title-main">Coronary artery bypass surgery</span> Surgical procedure to restore normal blood flow to an obstructed coronary artery

Coronary artery bypass surgery, also known as coronary artery bypass graft, is a surgical procedure to treat coronary artery disease (CAD), the buildup of plaques in the arteries of the heart. It can relieve chest pain caused by CAD, slow the progression of CAD, and increase life expectancy. It aims to bypass narrowings in heart arteries by using arteries or veins harvested from other parts of the body, thus restoring adequate blood supply to the previously ischemic heart.

<span class="mw-page-title-main">Great saphenous vein</span> Large, subcutaneous, superficial vein of the leg

The great saphenous vein(GSV), or long saphenous vein; ) is a large, subcutaneous, superficial vein of the leg. It is the longest vein in the body, running along the length of the lower limb, returning blood from the foot, leg and thigh to the deep femoral vein at the femoral triangle.

<span class="mw-page-title-main">Radial artery</span> Large forearm artery

In human anatomy, the radial artery is the main artery of the lateral aspect of the forearm.

<span class="mw-page-title-main">Cardiac surgery</span> Type of surgery performed on the heart

Cardiac surgery, or cardiovascular surgery, is surgery on the heart or great vessels performed by cardiac surgeons. It is often used to treat complications of ischemic heart disease ; to correct congenital heart disease; or to treat valvular heart disease from various causes, including endocarditis, rheumatic heart disease, and atherosclerosis. It also includes heart transplantation.

<span class="mw-page-title-main">Endarterectomy</span> Surgical procedure

Endarterectomy is a surgical procedure to remove the atheromatous plaque material, or blockage, in the lining of an artery constricted by the buildup of deposits. It is carried out by separating the plaque from the arterial wall.

<span class="mw-page-title-main">Internal thoracic artery</span> Artery of the thorax

In human anatomy, the internal thoracic artery (ITA), also known as the internal mammary artery, is an artery that supplies the anterior chest wall and the breasts. It is a paired artery, with one running along each side of the sternum, to continue after its bifurcation as the superior epigastric and musculophrenic arteries.

Hybrid coronary revascularization (HCR) or hybrid coronary bypass is a relatively new type of heart surgery that provides an alternative to traditional coronary artery bypass surgery (CABG) or percutaneous coronary intervention by combining the two into one operation. It is this combining aspect that "hybrid" refers to. HCR is one of several types of hybrid cardiac surgery; it is not to be confused with a MIDCAB procedure, which uses the smaller thoracotomy incision but does not involve coronary stenting.

<span class="mw-page-title-main">Right gastroepiploic artery</span>

The right gastroepiploic artery is one of the two terminal branches of the gastroduodenal artery. It runs from right to left along the greater curvature of the stomach, between the layers of the greater omentum, anastomosing with the left gastroepiploic artery, a branch of the splenic artery.

<span class="mw-page-title-main">Drug-eluting stent</span> Medical stent that releases drug

A drug-eluting stent (DES) is a thin tube that is used to treat narrowed arteries in medical procedures. It releases drugs to prevent the growth of scar tissue and reduce the risk of stent restenosis, which is the narrowing of the stented area of an artery after treatment. A drug-eluting stent is different from other types of stents because it has a coating that delivers medication directly to the arterial wall. A DES is often made of metal alloys and can be inserted into blocked or narrowed arteries through a catheter placed in a peripheral artery, such as in the arm or leg. DES is fully integrated with a catheter delivery system and is viewed as one integrated medical device.

Postperfusion syndrome, also known as "pumphead", is a constellation of neurocognitive impairments attributed to cardiopulmonary bypass (CPB) during cardiac surgery. Symptoms of postperfusion syndrome are subtle and include defects associated with attention, concentration, short-term memory, fine motor function, and speed of mental and motor responses. Studies have shown a high incidence of neurocognitive deficit soon after surgery, but the deficits are often transient with no permanent neurological impairment.

<span class="mw-page-title-main">Off-pump coronary artery bypass</span>

Off-pump coronary artery bypass or "beating heart" surgery is a form of coronary artery bypass graft (CABG) surgery performed without cardiopulmonary bypass as a treatment for coronary heart disease. It was primarily developed in the early 1990s by Dr. Amano Atsushi. Historically, during bypass surgeries, the heart is stopped and a heart-lung machine takes over the work of the heart and lungs. When a cardiac surgeon chooses to perform the CABG procedure off-pump, also known as OPCAB, the heart is still beating while the graft attachments are made to bypass a blockage.

<span class="mw-page-title-main">Coronary ischemia</span> Medical condition

Coronary ischemia, myocardial ischemia, or cardiac ischemia, is a medical term for a reduced blood flow in the coronary circulation through the coronary arteries. Coronary ischemia is linked to heart disease, and heart attacks. Coronary arteries deliver oxygen-rich blood to the heart muscle. Reduced blood flow to the heart associated with coronary ischemia can result in inadequate oxygen supply to the heart muscle. When oxygen supply to the heart is unable to keep up with oxygen demand from the muscle, the result is the characteristic symptoms of coronary ischemia, the most common of which is chest pain. Chest pain due to coronary ischemia commonly radiates to the arm or neck. Certain individuals such as women, diabetics, and the elderly may present with more varied symptoms. If blood flow through the coronary arteries is stopped completely, cardiac muscle cells may die, known as a myocardial infarction, or heart attack.

Minimally invasive cardiac surgery, also known as MICS CABG or the McGinn technique is heart surgery performed through several small incisions instead of the traditional open-heart surgery that requires a median sternotomy approach. MICS CABG is a beating-heart multi-vessel procedure performed under direct vision through an anterolateral mini-thoracotomy.

Vessel harvesting is a surgical technique that may be used in conjunction with a coronary artery bypass graft (CABG). For patients with coronary artery disease, a physician may recommend a bypass to reroute blood around blocked arteries to restore and improve blood flow and oxygen to the heart. To create the bypass graft, a surgeon will remove or "harvest" healthy blood vessels from another part of the body, often from the patient's leg or arm. This vessel becomes a graft, with one end attaching to a blood source above and the other end below the blocked area, creating a "conduit" channel or new blood flow connection across the heart.

<span class="mw-page-title-main">Reperfusion therapy</span> Restoring blood flow post-heart attack

Reperfusion therapy is a medical treatment to restore blood flow, either through or around, blocked arteries, typically after a heart attack. Reperfusion therapy includes drugs and surgery. The drugs are thrombolytics and fibrinolytics used in a process called thrombolysis. Surgeries performed may be minimally-invasive endovascular procedures such as a percutaneous coronary intervention (PCI), which involves coronary angioplasty. The angioplasty uses the insertion of a balloon and/or stents to open up the artery. Other surgeries performed are the more invasive bypass surgeries that graft arteries around blockages.

<span class="mw-page-title-main">Ischemic cardiomyopathy</span> Medical condition

Ischemic cardiomyopathy is a type of cardiomyopathy caused by a narrowing of the coronary arteries which supply blood to the heart. Typically, patients with ischemic cardiomyopathy have a history of acute myocardial infarction, however, it may occur in patients with coronary artery disease, but without a past history of acute myocardial infarction. This cardiomyopathy is one of the leading causes of sudden cardiac death. The adjective ischemic means characteristic of, or accompanied by, ischemia — local anemia due to mechanical obstruction of the blood supply.

<span class="mw-page-title-main">External support</span>

In cardiac surgery and vascular surgery, external support is a type of scaffold made of metal or plastic material that is inserted over the outside of the vein graft in order to decrease the intermediate and late vein graft failure after bypass surgery.

Uwe Klima is UAE based professor of surgery and a faculty member at the Hannover Medical School, Germany. He also is the medical and managing director at German Heart Centre, Dubai.

John D. Puskas is an American researcher, author, inventor and cardiovascular surgeon. As of 2022, he is Professor, Cardiovascular Surgery, Icahn School of Medicine at Mount Sinai, and chairman, Department of Cardiovascular Surgery at Mount Sinai Morningside, Mount Sinai Beth Israel and Mount Sinai West. He holds 11 U.S. patents and co-founded the International Coronary Congress and the International Society for Coronary Artery Surgery. He is credited by ResearchGate with 330 publications and 15,234 citations and as of 2022 Scopus reports an h-index of 62. Puskas is known for advancing coronary artery bypass (CABG) surgery by refining surgical techniques for all-arterial, off-pump CABG and inventing finer instruments to be used for advanced coronary bypass surgical procedures. He is credited with performing the first totally thoracoscopic bilateral pulmonary vein isolation procedure. He is the co-editor of State of the Art Surgical Coronary Revascularization, the first textbook solely devoted to coronary artery surgery.

References

  1. Goldman S, Zadina K, Moritz T, Ovitt T, Sethi G, Copeland JG, Thottapurathu L, Krasnicka B, Ellis N, Anderson RJ, Henderson W (December 2004). "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 (11): 2149–56. doi: 10.1016/j.jacc.2004.08.064 . PMID   15582312.
  2. 1 2 Fitzgibbon, GM; Kafka, HP; Leach, AJ; Keon, WJ; Hooper, GD; Burton, JR (September 1996). "Coronary bypass graft fate and patient outcome: angiographic follow-up of 5,065 grafts related to survival and reoperation in 1,388 patients during 25 years". Journal of the American College of Cardiology. 28 (3): 616–26. doi: 10.1016/0735-1097(96)00206-9 . PMID   8772748.
  3. Hess CN, Lopes RD, Gibson CM, Hager R, Wojdyla DM, Englum BR, Mack MJ, Califf RM, Kouchoukos NT, Peterson ED, Alexander JH (October 2014). "Saphenous vein graft failure after coronary artery bypass surgery: insights from PREVENT IV". Circulation. 130 (17): 1445–51. doi:10.1161/CIRCULATIONAHA.113.008193. PMC   4206593 . PMID   25261549.
  4. McKavanagh P, Yanagawa B, Zawadowski G, Cheema A (December 2017). "Management and Prevention of Saphenous Vein Graft Failure: A Review". Cardiol Ther. 6 (2): 203–223. doi:10.1007/s40119-017-0094-6. PMC   5688971 . PMID   28748523.
  5. Halabi AR, Alexander JH, Shaw LK, Lorenz TJ, Liao L, Kong DF, Milano CA, Harrington RA, Smith PK (November 2005). "Relation of early saphenous vein graft failure to outcomes following coronary artery bypass surgery". Am. J. Cardiol. 96 (9): 1254–9. doi:10.1016/j.amjcard.2005.06.067. PMID   16253593.
  6. Lichtenwalter C, de Lemos JA, Roesle M, Obel O, Holper EM, Haagen D, et al. (September 2009). "Clinical presentation and angiographic characteristics of saphenous vein graft failure after stenting: insights from the SOS (stenting of saphenous vein grafts) trial". JACC Cardiovasc Interv. 2 (9): 855–60. doi: 10.1016/j.jcin.2009.06.014 . PMID   19778774.
  7. Lardenoye, JH; de Vries, MR; Löwik, CW; Xu, Q; Dhore, CR; Cleutjens, JP; van Hinsbergh, VW; van Bockel, JH; Quax, PH (4 October 2002). "Accelerated atherosclerosis and calcification in vein grafts: a study in APOE*3 Leiden transgenic mice". Circulation Research. 91 (7): 577–84. CiteSeerX   10.1.1.551.5044 . doi:10.1161/01.res.0000036901.58329.d7. PMID   12364385. S2CID   566476.
  8. Angelini, GD; Passani, SL; Breckenridge, IM; Newby, AC (December 1987). "Nature and pressure dependence of damage induced by distension of human saphenous vein coronary artery bypass grafts". Cardiovascular Research. 21 (12): 902–7. doi:10.1093/cvr/21.12.902. PMID   3502670.
  9. Manchio, JV; Gu, J; Romar, L; Brown, J; Gammie, J; Pierson RN, 3rd; Griffith, B; Poston, RS (June 2005). "Disruption of graft endothelium correlates with early failure after off-pump coronary artery bypass surgery". The Annals of Thoracic Surgery. 79 (6): 1991–8. doi:10.1016/j.athoracsur.2004.12.054. PMID   15919298.{{cite journal}}: CS1 maint: numeric names: authors list (link)
  10. Allaire, E; Clowes, AW (February 1997). "Endothelial cell injury in cardiovascular surgery: the intimal hyperplastic response". The Annals of Thoracic Surgery. 63 (2): 582–91. doi:10.1016/S0003-4975(96)01045-4. PMID   9033355.
  11. Nwasokwa, ON (1 October 1995). "Coronary artery bypass graft disease". Annals of Internal Medicine. 123 (7): 528–45. doi:10.7326/0003-4819-123-7-199510010-00009. PMID   7661498. S2CID   28240233.
  12. Schwartz, SM; deBlois, D; O'Brien, ER (September 1995). "The intima. Soil for atherosclerosis and restenosis". Circulation Research. 77 (3): 445–65. doi:10.1161/01.res.77.3.445. PMID   7641318.
  13. Zhang, L; Peppel, K; Brian, L; Chien, L; Freedman, NJ (December 2004). "Vein graft neointimal hyperplasia is exacerbated by tumor necrosis factor receptor-1 signaling in graft-intrinsic cells". Arteriosclerosis, Thrombosis, and Vascular Biology. 24 (12): 2277–83. doi: 10.1161/01.ATV.0000147766.68987.0d . PMID   15486311.
  14. Stary, HC; Blankenhorn, DH; Chandler, AB; Glagov, S; Insull W, Jr; Richardson, M; Rosenfeld, ME; Schaffer, SA; Schwartz, CJ; Wagner, WD (January 1992). "A definition of the intima of human arteries and of its atherosclerosis-prone regions. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association". Circulation. 85 (1): 391–405. doi: 10.1161/01.cir.85.1.391 . PMID   1728483.
  15. Yahagi, K; Kolodgie, FD; Otsuka, F; Finn, AV; Davis, HR; Joner, M; Virmani, R (February 2016). "Pathophysiology of native coronary, vein graft, and in-stent atherosclerosis". Nature Reviews. Cardiology. 13 (2): 79–98. doi:10.1038/nrcardio.2015.164. PMID   26503410. S2CID   205471779.
  16. Ramos De Souza, Domingos; Dashwood, Michael R.; Samano, Ninos (October 2017). "Saphenous vein graft harvesting and patency: No-touch harvesting is the answer". The Journal of Thoracic and Cardiovascular Surgery. 154 (4): 1300–1301. doi: 10.1016/j.jtcvs.2017.02.010 . PMID   28918921.
  17. Samano, Ninos; Souza, Domingos; Dashwood, Michael R (June 2021). "Saphenous veins in coronary artery bypass grafting need external support". Asian Cardiovascular and Thoracic Annals. 29 (5): 457–467. doi:10.1177/0218492320980936. ISSN   0218-4923. PMC   8167919 . PMID   33307718.
  18. Authors/Task Force, members.; Windecker, S; Kolh, P; Alfonso, F; Collet, JP; Cremer, J; Falk, V; Filippatos, G; Hamm, C; Head, SJ; Jüni, P; Kappetein, AP; Kastrati, A; Knuuti, J; Landmesser, U; Laufer, G; Neumann, FJ; Richter, DJ; Schauerte, P; Sousa Uva, M; Stefanini, GG; Taggart, DP; Torracca, L; Valgimigli, M; Wijns, W; Witkowski, A (1 October 2014). "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)". European Heart Journal. 35 (37): 2541–619. doi: 10.1093/eurheartj/ehu278 . PMID   25173339.
  19. Hillis LD, Smith PK, Anderson JL, Bittl JA, Bridges CR, Byrne JG, et al. (December 2011). "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 (23): e652–735. doi: 10.1161/CIR.0b013e31823c074e . PMID   22064599.
  20. European Stroke, Organisation.; Tendera, M; Aboyans, V; Bartelink, ML; Baumgartner, I; Clément, D; Collet, JP; Cremonesi, A; De Carlo, M; Erbel, R; Fowkes, FG; Heras, M; Kownator, S; Minar, E; Ostergren, J; Poldermans, D; Riambau, V; Roffi, M; Röther, J; Sievert, H; van Sambeek, M; Zeller, T; ESC Committee for Practice, Guidelines. (November 2011). "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)". European Heart Journal. 32 (22): 2851–906. doi: 10.1093/eurheartj/ehr211 . PMID   21873417.
  21. Anderson, JL; Halperin, JL; Albert, NM; Bozkurt, B; Brindis, RG; Curtis, LH; DeMets, D; Guyton, RA; Hochman, JS; Kovacs, RJ; Ohman, EM; Pressler, SJ; Sellke, FW; Shen, WK (2 April 2013). "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 (13): 1425–43. doi:10.1161/CIR.0b013e31828b82aa. PMC   4492473 . PMID   23457117.
  22. Souza, DS; Dashwood, MR; Tsui, JC; Filbey, D; Bodin, L; Johansson, B; Borowiec, J (April 2002). "Improved patency in vein grafts harvested with surrounding tissue: results of a randomized study using three harvesting techniques". The Annals of Thoracic Surgery. 73 (4): 1189–95. doi: 10.1016/s0003-4975(02)03425-2 . PMID   11996262.
  23. Souza, DS; Johansson, B; Bojö, L; Karlsson, R; Geijer, H; Filbey, D; Bodin, L; Arbeus, M; Dashwood, MR (August 2006). "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". The Journal of Thoracic and Cardiovascular Surgery. 132 (2): 373–8. doi: 10.1016/j.jtcvs.2006.04.002 . PMID   16872965.
  24. Kopjar T, Dashwood MR (February 2016). "Endoscopic Versus "No-Touch" Saphenous Vein Harvesting for Coronary Artery Bypass Grafting: A Trade-Off Between Wound Healing and Graft Patency". Angiology. 67 (2): 121–32. doi:10.1177/0003319715584126. PMID   25972395. S2CID   5086303.
  25. Deppe, AC; Liakopoulos, OJ; Choi, YH; Slottosch, I; Kuhn, EW; Scherner, M; Stange, S; Wahlers, T (March 2013). "Endoscopic vein harvesting for coronary artery bypass grafting: a systematic review with meta-analysis of 27,789 patients". The Journal of Surgical Research. 180 (1): 114–24. doi:10.1016/j.jss.2012.11.013. PMID   23218736.
  26. Harskamp, RE; Alexander, JH; Schulte, PJ; Brophy, CM; Mack, MJ; Peterson, ED; Williams, JB; Gibson, CM; Califf, RM; Kouchoukos, NT; Harrington, RA; Ferguson TB, Jr; Lopes, RD (August 2014). "Vein graft preservation solutions, patency, and outcomes after coronary artery bypass graft surgery: follow-up from the PREVENT IV randomized clinical trial". JAMA Surgery. 149 (8): 798–805. doi:10.1001/jamasurg.2014.87. PMC   4332522 . PMID   25073921.
  27. Taggart, DP; Ben Gal, Y; Lees, B; Patel, N; Webb, C; Rehman, SM; Desouza, A; Yadav, R; De Robertis, F; Dalby, M; Banning, A; Channon, KM; Di Mario, C; Orion, E (June 2015). "A Randomized Trial of External Stenting for Saphenous Vein Grafts in Coronary Artery Bypass Grafting" (PDF). The Annals of Thoracic Surgery. 99 (6): 2039–45. doi:10.1016/j.athoracsur.2015.01.060. hdl: 10044/1/53822 . PMID   25886810. S2CID   25323596.
  28. Taggart DP, Amin S, Djordjevic J, Oikonomou EK, Thomas S, Kampoli AM, Sabharwal N, Antoniades C, Krasopoulos G (May 2017). "A prospective study of external stenting of saphenous vein grafts to the right coronary artery: the VEST II study". Eur J Cardiothorac Surg. 51 (5): 952–958. doi: 10.1093/ejcts/ezw438 . PMID   28379404.
  29. Meirson, T; Orion, E; Di Mario, C; Webb, C; Patel, N; Channon, KM; Ben Gal, Y; Taggart, DP (October 2015). "Flow patterns in externally stented saphenous vein grafts and development of intimal hyperplasia". The Journal of Thoracic and Cardiovascular Surgery. 150 (4): 871–8. doi: 10.1016/j.jtcvs.2015.04.061 . hdl: 10044/1/25844 . PMID   26242834.
  30. Eefting, D; de Vries, MR; Grimbergen, JM; Karper, JC; van Bockel, JH; Quax, PH (February 2010). "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". Journal of Vascular Surgery. 51 (2): 429–37. doi: 10.1016/j.jvs.2009.09.026 . PMID   20036101.
  31. Quax, PH; Lamfers, ML; Lardenoye, JH; Grimbergen, JM; de Vries, MR; Slomp, J; de Ruiter, MC; Kockx, MM; Verheijen, JH; van Hinsbergh, VW (30 January 2001). "Adenoviral expression of a urokinase receptor-targeted protease inhibitor inhibits neointima formation in murine and human blood vessels". Circulation. 103 (4): 562–9. doi: 10.1161/01.cir.103.4.562 . PMID   11157723.
  32. Karper, JC; de Vries, MR; van den Brand, BT; Hoefer, IE; Fischer, JW; Jukema, JW; Niessen, HW; Quax, PH (May 2011). "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". Arteriosclerosis, Thrombosis, and Vascular Biology. 31 (5): 1033–40. doi: 10.1161/ATVBAHA.111.223271 . hdl: 1871/20163 . PMID   21330606.
  33. Pradhan-Nabzdyk, L; Huang, C; LoGerfo, FW; Nabzdyk, CS (September 2014). "Current siRNA targets in the prevention and treatment of intimal hyperplasia". Discovery Medicine. 18 (98): 125–32. PMC   4265021 . PMID   25227753.