Asian Cardiovasc Thorac Ann 2008;16:331-336
© 2008 Asia Publishing EXchange Ltd
Pathophysiology of Aortocoronary Saphenous Vein Bypass Graft Disease
Seyed-Ahmad Hassantash, MD,
Behnood Bikdeli, MD,
Shadi Kalantarian, MD,
Maryam Sadeghian, MD,
Haleh Afshar, MD
Modarres Cardiovascular Research Center, Shaheed Beheshti University of Medical Sciences, Tehran, Iran
For reprint information contact: Seyed-Ahmad Hassantash, MD, Tel: 98 21 2208 3106, Fax: 98 21 2208 3106, Email: sahassan{at}pol.net, Department of Cardiovascular Surgery, Modarres Medical Center, Shaheed Beheshti University of Medical Sciences, Saadat-Abad, Tehran, Iran.
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ABSTRACT
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Aortocoronary saphenous vein bypass grafting relieves anginal pain in patients with coronary artery disease. However, its effectiveness is limited due to graft failure; the 10-year patency rate is 50%–60%. Early, 1-year and late graft failure may be due to thrombosis, fibrointimal hyperplasia and atherosclerosis, respectively. There is general agreement that vein graft atherosclerosis differs from arterial lesions in terms of temporal and histological changes. Vein graft atherosclerosis is more rapid, with diffuse concentric changes and a less noticeable fibrous cap, making venous plaques more vulnerable to rupture and subsequent thrombus formation. Despite progress in understanding the pathophysiology, some aspects of vein graft atherosclerosis need to be clarified. This review focuses on the pathophysiologic aspects of this widespread, costly and disabling disease, with emphasis on late graft occlusion and distinctions between arterial and venous atherosclerosis in terms of histology, pathophysiology and risk factors.
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INTRODUCTION
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Coronary artery disease is the leading cause of mortality and morbidity worldwide. Many of the large number of patients suffering from this disease will need revascularization, mainly due to recurrent angina. Percutaneous revascularization techniques and coronary artery bypass grafting (CABG) are universally applied in such patients. Although the recent advent of drug-eluting stents has shown promise, CABG continues to be one of the 2 main treatments employed.1–7 Coronary artery bypass grafting can successfully alleviate anginal pain and improve clinical short- and long-term outcomes in many patients with coronary artery disease.8–10 Arterial grafts are superior for CABG; however, adequate arterial conduits are not always available. In contrast, saphenous vein grafts (SVGs) are plentiful and easily harvested, thus commonly used as CABG conduits.11–13
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HISTOLOGY OF NORMAL SAPHENOUS VEIN
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The native saphenous vein intima is composed of a continuous layer of endothelial cells lying on a fenestrated basement membrane embedded with a fragmented internal elastic lamina. Three layers of smooth muscles comprise the media, each separated by loose connective tissue and elastic fibers. The middle muscular layer, which is arranged in a circular fashion, is most extensive at the insertion points of the valves and leaflets. Adventitia, the outermost layer, consists of longitudinally arranged smooth muscle cells (SMCs), collagen fibers and a network of elastin fibers, in addition to vascular and nerve supplies to the vessel.11,14–16 There are definite features specific to saphenous veins: they are more muscular and elastin rich than a typical vein wall.17 Untouched native saphenous veins may show mild intimal and/or medial fibrosis even before grafting. Studies on unused harvested grafts revealed that approximately 1% of saphenous veins have > 50% stenosis before grafting.18,19
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GRAFT FAILURE
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Some investigators suggest that there is minimal damage to the endothelium and SMCs following SVG harvesting.20 However, numerous studies have indicated that saphenous veins may undergo remodeling before and after grafting. Surgical preparation techniques modulate the phenotype of the SMC and may cause SMC migration, leading to intimal thickening. Matrix metalloproteinase activity is also enhanced after preparation.21 There are other pathogenic mechanisms leading to remodeling of the newly grafted vein. Surgical manipulation and distension before anastomosis leads to loss of endothelial integrity and the antithrombogenic attributes of the endothelium, rendering the vein prone to subsequent occlusive intimal hyperplasia and/or thrombus formation.22 Furthermore, the vasa vasorum and nervous network of the veins are essentially divided during harvesting. This makes the SVG dependent solely on diffusion for the first week after implantation. It may take up to 6 months for adequate circulation to the grafted vessel to be reestablished.23–28 Ischemic insult and diminished NO and adenosine production in isolation may trigger SMC proliferation.29 In an experimental model designed to evaluate the effects of vein-to-vein grafting, Zou and colleagues30 demonstrated that intimal hyperplasia does not occur in vein-to-vein isografts, although leukocyte infiltration may be seen. Thus it can be stated that pathologic changes seen in SVG atherosclerosis are mostly a function of the hemodynamic and physiochemical changes due to veins replacing arteries, rather than the process of harvesting and grafting the vessel. The SVG is prone to obliteration by 3 distinct mechanisms (Figure 1
): within the 1st month postoperatively, thrombosis predominates; fibrointimal hyperplasia is the most common finding in specimens one month to one year old; and atherosclerosis is the major cause of lesions older than 1 year. Intimal hyperplasia is the foundation for subsequent graft atheroma formation.
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Figure 1. Evolutional of changes in saphenous veins used as aortocoronary bypass conduits. C/P = chest pain, DOE = dyspnea on exertion, DVT = deep vein thrombosis, EKG = electrocardiogram, MMP = matrix metalloproteinase, SMC = smooth muscle cell, SV = saphenous vein.
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EARLY GRAFT FAILURE
Early graft failure due to thrombotic complications is attributable to technical errors during harvesting and anastomosis or compromised anatomic runoff.18,19,31,32 It occurs in 15%–18% of SVGs as a result of thrombosis during the 1st month.11,33,34 Early thrombotic complications are caused by a reduction of tissue plasminogen activator, attenuation of thrombomodulin and reduced expression of heparan sulfate in vein grafts compared to arteries.35
MIDTERM GRAFT FAILURE
Fibrointimal hyperplasia is the main pathologic finding responsible for occlusive stenosis from the 1st month to the 1st year, which accounts for occlusion of an additional 15% to 30% of SVGs.36,37 In general, intimal hyperplasia per se does not lead to significant stenosis; however, it serves as the foundation for subsequent graft atheroma. Smooth muscle cell migration and proliferation in response to the release of a variety of mediators, growth factors, and cytokines by the injured endothelium, platelets and activated macrophages is the key event in the development of neointimal hyperplasia. Also, diminished production of endothelial NO, prostaglandin I2 and adenosine will lead to enhanced SMC proliferation.12,18,29,38–40 Surgical, traumatic and ischemic insults together with changes in the flow pattern within the vessel (shear stress) may be responsible for changes occurring at this stage. Grafted vessels are exposed to almost 10 times the mechanical pressure they were adapted to (arterial vs. venous blood pressure). This serves as a potent stimulator of SMC proliferation. What is more, increased levels of intracellular adhesion molecule-1, vascular cell adhesion molecule-1, and monocyte chemotactic protein-1 after encountering arterial flow patterns will facilitate leukocyte-endothelial interactions so that leukocyte infiltration of the lesions will ensue.30 The distal site of anastomosis (junction between graft and host vessel) is a frequent site of late graft failure; an effect that is partly related to adaptive responses to hemodynamic factors, namely wall shear stress.41,42
LATE GRAFT FAILURE
Later in the course of vessel wall remodeling, intimal fibrosis progresses at the cost of a reduction in cellularity.18,30,35 This may be attributable to progressive SMC apoptosis.40 However, Hilker and colleagues43 did not find any correlation between the cellularity and timing of the lesions. Perivascular fibroblasts may also be involved in neointimal formation and matrix deposition. These cells may exhibit contractile elements while migrating from the adventitia towards the media.11,44 The role of immune cells in neointimal formation has also been emphasized in many studies. Macrophages are found in the intima, while T-lymphocytes are evident in the adventitia of neointimal lesions, with a predominance of CD4+ cells.45–47 Atherosclerosis accounts for most stenotic complications after the 1st year, and there is ample evidence that the 10-year SVG patency rate is no more than 50%–60%.18,35,48,49 Although it is said that vein graft atherosclerosis is accelerated compared to that of arteries, it is unlikely that a fully evolved plaque would appear earlier than 3–5 years from implantation.31,36,50 Additionally, these lesions resemble those of experimental models of immune-mediated atherosclerosis, suggesting the immune system plays a role in these lesions.50–52
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VENOUS VS ARTERIAL ATHEROSCLEROSIS
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Venous atherosclerotic plaques share most of the pathologic features of native coronary atherosclerosis, and some investigators believe that little difference exists between the morphologic appearance of SVG plaques and those of native coronary arteries.53 The plaques are established in the ground of intimal hyperplastic tissue. A thin fragile fibrous cap, proliferating SMCs, foam cells (of macrophage or SMC origin), a variety of inflammatory cells including macrophages, lymphocytes and even plasma cells, giant cells, dendritic cells along with extracellular lipid droplets, neovasculature, and modified moieties of matrix components including glycosaminoglycans and proteoglycans can be detected in such lesions.18,46,47,50,54–58 Interestingly, red blood cell membranes may be the source of internalized lipids in macrophages.59 Calcification may be superimposed onto SVG atherosclerotic plaques, although its presence and significance have been debated.18,46,60–64 Nevertheless, it has been shown that there are certain distinctions between venous and arterial atherosclerotic lesions. In contrast to arterial atheroma, venous plaques are more concentric and diffuse, and the fibrous cap is less fully developed, making them more vulnerable to rupture or disruption and ensuing thrombus formation.18,35,53 Compared to arteries, lipolysis is sluggish in veins, including the saphenous vein. Also, veins have a more powerful system of lipid biosynthesis and uptake. This partly accounts for the accelerated formation of SVG atherosclerosis.65,66 As time passes, dense fibrous tissue is increased proportionally so that venous lesions resemble those of native coronary atherosclerosis.60 Recently, certain infectious agents have been proposed to play a role in atherosclerosis in both arteries and vein grafts; most studies in vein grafts have focused on the presence of Chlamydia pneumoniae in atherosclerotic plaques.65–67 A role for other infectious agents such as Helicobacter pylori remains elusive.
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COMPLICATIONS OF VEIN GRAFT ATHEROMA
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A series of events may later complicate atherosclerotic lesions. Of note, is aneurysmal dilatation which in a series of patients correlated with thrombosed grafts in all cases.68 In general, atheroembolism from the diseased vein is the major cause of mortality and morbidity mandating revascularization therapy.18,35 Also, plaque rupture, which is more commonly seen in vein grafts, may be a pivotal factor in late thrombosis of the lesions.69,70 With lipid accumulation, tensile stress is locally imbalanced within the plaque, leading to rupture and subsequent thrombus formation.71 Sometimes multiple ruptured plaques may be seen, particularly in diabetic patients.61,72
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RISK FACTORS
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Risk factors for SVG atherosclerosis are almost identical to those of native coronary atheroma formation.18,73 The only exception is hypertension which correlates with intimal hyperplasia but probably not with atherosclerosis in vein grafts; although ruptured plaques may be seen more often in patients with hypertension.18,36,72,74 Table 1 summarizes the main risk factors associated with arterial and vein graft atherosclerosis.
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CHOICE FOR REVASCULARIZATION
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All the above-mentioned factors lead to delayed graft stenosis or occlusion, mandating redo CABG or percutaneous interventions. Percutaneous coronary interventions have considerable shortcomings as a treatment modality for vein graft stenosis. There are poor in-hospital and long-term outcomes of angioplasty. Saphenous vein graft stenting is also problematic because distal embolization, no-reflow phenomenon, higher rates of peri-procedural myocardial infarction, and restenosis (in at least 30% of patients) may ensue. Recent advances in the use of embolic protection devices for selected patients have minimized complications associated with embolization of the lesions. However, routine use of such devices is not yet feasible due to high cost and technical complexity.75,76 Another problem might arise from the involvement of angiographically insignificant lesions. Repeat CABG directed at SVG degeneration and progression of native atherosclerotic disease also carries substantially greater perioperative mortality and morbidity in conjunction with worse short and long-term outcomes than primary procedures. So far, no randomized controlled trial has compared redo CABG with percutaneous interventions for treatment of SVG disease.18,35,77–80
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CONCLUSION
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A thorough understanding of the mechanisms leading to SVG stenosis or atherosclerosis will facilitate finding more robust therapeutic strategies to reduce the need for percutaneous interventions or redo CABG. To date, no studies have compared electron microscopic histopathologic findings with angiographic features. Such investigations may provide valuable clues for better clarification of extraluminal atherosclerosis. As new research and clinical experience broadens our knowledge of the pathogenesis and pathophysiology of vein graft atherosclerosis, it will not seem farfetched to introduce novel treatment options against this widespread, costly, and disabling disease.
Presented at the 7th Annual Research Seminar of the Iranian Medical Sciences’ Students, Tehran, June 2006.
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ACKNOWLEDGMENTS
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The authors would like to thank Dr Mohammad Varahram, Dr Ali Anisian and Mr Mohsen Ahoo Ghalandari from Students Research Committee for their kind support, and Dr Leonard Stuart Lilly from Harvard Medical School for his valuable comments and review of the manuscript.
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ABSTRACT
INTRODUCTION
