Annals of Vascular Surgery
Volume 21, Issue 6 , Pages 695-703, November 2007

The Natural History of Stenoses within Lower Limb Arterial Bypass Grafts Using a Graft Surveillance Program

Department of Vascular Surgery, Manchester Royal Infirmary, Manchester, UK

Article Outline

Graft surveillance aims to identify those grafts that are at risk of failure as intervention in a patent but failing graft results in improved long-term patency and limb salvage rates compared to rescue of an occluded graft. Controversy exists as to which types of graft benefit the most from surveillance and whether patient factors such as diabetes and smoking status have an effect on graft survival. Our aims were (1) to clarify the natural history of midterm graft failure as a consequence of myointimal hyperplasia and (2) to identify which patients and grafts are at a higher risk of failure and at what time points this is most prevalent. Serial vascular laboratory and clinical data of 212 infrainguinal lower limb grafts in 197 patients were analyzed. Follow-up within the surveillance program was by focused examination with color flow duplex ultrasound at 0, 1, 3, 6, 12, and 18 months with respect to surgery. Outcomes were correlated with retrospectively collected data regarding patient demographics, smoking status, concurrent medication, comorbidity, and operative factors such as distal target vessel and conduit. During the program, 21.6% of grafts occluded. Overall, 16% of grafts underwent a salvage procedure, 40.5% of which were carried out at the 6-month time point. There were 56.6% of occlusions preceded by a stenotic lesion. Primary occlusions accounted for 95.9% in the prosthetic group and 66.5% in the femorocrural group. As a group, vein grafts were more likely to develop a progressive stenosis prior to occlusion, with 58.3% in this group predated by a stenotic lesion. Fewer than 75% of stenoses were common and had a variable natural history, with over 40% resolving or failing to progress. Throughout the study period, 56.2% of grafts remained stenosis-free. Stenoses were more common at the proximal anastomosis in the vein graft cohort. There were low rates of significant stenoses within the prosthetic group. These lesions were more likely to occur at the distal anastomosis but were poor predictors of occlusion. Statin use postoperatively was protective against the development of significant stenosis and occlusions, particularly in the above-knee grafts (p = 0.03). Surprisingly, preoperative smoking status was predictive of neither occlusion nor development of significant stenosis. The presence of diabetes was not predictive of poor outcome. Our findings suggest that graft surveillance is a valid method for detecting the presence of significant stenoses in vein grafts at high risk of failure without intervention. Despite the intensive follow-up, the program failed to detect lesions prior to occlusion in a large percentage of prosthetic and femorocrural grafts, so perhaps this group is poorly served by graft surveillance.

 

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Introduction 

Arterial bypass surgery is a well-established treatment modality in peripheral arterial disease being performed for aneurysmal disease, trauma, and, most frequently, ischemia. Although early patency is routinely achieved, the life span of the graft is highly variable, with a significant proportion failing in subsequent years. Graft failure remains a significant clinical problem for surgeons, health care–delivery systems, and patients. Arterial bypass remains the gold standard for infrainguinal occlusive disease. With continual improvements in surgical and anesthetic technique and graft materials, patients can be offered safe and effective treatment for critical limb ischemia and disabling claudication.1

The attrition of functioning vein grafts due to progressive stenosis remains the Achilles heel of peripheral arterial reconstruction. Much work has been done in improving patency rates and long-term outcomes, but this has been predominantly through improved anastomotic techniques such as spatulating the graft, decreasing early graft failure rates to <5%, and aggressive medical management of atherosclerosis, with a reduction in late graft failure.2, 3 Occlusion beyond the first year is most often the consequence of progression of atherosclerotic plaques sufficient to compromise graft inflow or outflow.1 Midterm graft failure usually occurs between 3 and 18 months and is responsible for 80% of clinically significant graft occlusions.2, 3 Midterm graft failure is becoming more prominent because both advancements in operative technique and improvements in the medical management of arteriosclerosis have resulted in a reduction in the proportions of early and late graft failure, respectively. Despite this, no effective pharmacological prophylaxis or treatment is yet available. The process responsible for the majority of midterm graft failures is myointimal hyperplasia. This process is characterized by progressive luminal encroachment of cellular components of the donor or target vessel as a consequence of arterial injury, compliance mismatch, and the shear forces of turbulent flow.4, 5, 6, 7

Prophylaxis of midterm graft failure by graft surveillance programs, aiming to identify grafts at risk, has been an attractive option since the early 1980s. However, some studies have shown variable results with routine graft surveillance programs, reporting little difference in limb salvage rates when compared to clinical monitoring alone.2, 8 Central to the rationale of graft surveillance is that early detection of graft stenoses and preemptive treatment confer a prognostic benefit to the patient, at least in terms of graft patency but, more importantly, limb salvage. This is particularly important through the time when midterm graft failure occurs as it is during this period that healing of amputation sites, ischemic ulcers, and collateralization occur. Occlusion during this period frequently necessitates reintervention, often with dismal outcome.9

Salvage of an occluded bypass graft often has disappointing results, with 2-year patency rates after successful revision reported to be as low as 19%.10, 11 However, these studies highlighted the contrasting fates of occluded grafts and those which were patent but contained a significant stenosis when aggressive rescue strategies were employed. At 2 years, a salvaged, thrombosed vein graft has 7% patency and a 44% limb salvage rate, while revision of a failing but patent graft has 81% patency and a 77% salvage rate.12, 13

Clinical examination and patient history are poor indicators of graft function, and several studies have shown that duplex ultrasound reliably identifies stenotic lesions in bypass grafts, removing the need for invasive follow-up with angiography.14, 15, 16, 17 Ankle-brachial pressure index (ABPI) is also a relatively insensitive tool for determining the progression of lower extremity disease or graft failure.18, 19, 20, 21 These techniques have been superseded by duplex scanning, which has been shown to improve graft patency by identification and correction of significant graft lesions.13, 22, 23, 24, 25

However, many authors have questioned the utility of graft surveillance in prosthetic grafts given that they uncommonly develop intragraft lesions, whereas these are common in autologous conduits.2, 26 Some centers have challenged this rationale, advocating prosthetic graft surveillance, particularly for below-knee grafts and for monitoring inflow and outflow.27, 28 The majority of vein grafts with a stenosis of 75% or more eventually occlude. Therefore, this has become the widely accepted threshold for intervention.29, 30 In one study, 65% of grafts which eventually occluded had an associated ≥75% stenosis, while only 12% of grafts with no previous evidence of stenosis failed.31

Factors predictive of graft failure remain poorly defined but include smoking,32 inflow and outflow disease, a crural target vessel,1 and the use of anticoagulants.33

This study set out, firstly, to clarify the natural history of midterm graft failure as a consequence of myointimal hyperplasia in prosthetic and vein bypass grafts of the lower limb and, secondly, to identify which patients and grafts are at an increased risk of failing and at which time points this is most prevalent.

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Methods 

Between February 1998 and September 2004 patients undergoing lower limb arterial bypass surgery for occlusive disease were prospectively recruited to the graft surveillance program. There were 585 grafts originally included. To allow for comparison between grafts and ease of data interpretation, only those grafts with a proximal anastomosis to the superficial or common femoral arteries were assessed. Those grafts where the proximal anastomosis was elsewhere in the arterial tree, crossover grafts, and composite grafts were excluded. This resulted in serial vascular laboratory and clinical data of 357 grafts in 297 patients, 220 of whom were men, with a median age of 68 years (range 40-90) being initially included. Those grafts with incomplete data sets were then removed from the final analysis, resulting in a cohort of 212 grafts in 197 patients. The study group thus consisted of five cohorts: femoral to above-knee popliteal vein and prosthetic grafts (AKV and AKP, respectively), below-knee popliteal vein and prosthetic grafts (BKV and BKP, respectively), and femorocrural vein grafts (FCV). In these grafts, data were analyzed only up to the first episode of thrombosis or development of a significant stenosis.

Operative technique varied between surgeons, but all vein grafts were performed using the reversed technique. Single long saphenous vein was the conduit used in the majority of vein bypasses. Short saphenous vein or upper limb superficial veins were only used in a very small number of cases. Expanded polytetrafluoroethylene (ePTFE) was only used in patients with inadequate autologous vein. Intraoperative assessment of grafts with duplex scanning was not routinely used. Postoperative anticoagulation was at the discretion of the operating surgeon; the majority of patients were medicated with low–molecular weight heparin until mobile. Antiplatelet therapy was not discontinued prior to surgery.

All patients enrolled in the graft surveillance program had a routine 6-week postoperative clinic visit. Follow-up within the surveillance program was by focused examination, including bilateral pre- and postexercise ABPI and color flow duplex ultrasound scanning of the graft and its inflow and outflow at 0, 1, 3, 6, 12, and 18 months with respect to surgery. The first scan occurred postoperatively but during the same admission. Color duplex scanning was carried out by five experienced clinical vascular scientists using an ATL 5000 ultrasonic duplex scanner (Antares, Scotts Valley, CA), and stenoses were graded according to the peak systolic velocity ratio (PSVR) according to published criteria.33 PSVRs of >3.5, 2.5-3.5, and <2.5 were used to indicate >75%, 50-75%, and <50% stenosis, respectively. Significant lesions were described as those having a stenosis of ≥75%. Patients were discharged from follow-up after 18 months. Any further review was based on clinical need.

Primary outcomes were graft occlusion, development of a significant stenosis, lower limb amputation, and death. Secondary outcomes were patency and the development of a stenosis of any degree. These outcomes were correlated with retrospectively collected information regarding age, sex, smoking status, concurrent medication, hypercholesterolemia, diabetes, and operative factors such as crural target vessel and conduit. Patient demographics with respect to graft type are shown in Table I. Demographic differences were assessed by one-way analysis of variance (StatsDirect, Altrincham, UK). Although there appear to be some differences between the five groups, these failed to reach statistical significance, with p > 0.05 in each case.

Table I. Patient demographics
AKVAKPBKVBKPFCVTotal
Number (% of total)78 (36.8)40 (18.9)54 (25.5)9 (4.2)31 (14.6)212 (100)
Male:female56:2227:1344:108:122:9157:55
Median age, years (range)67 (44-90)67 (44-75)69 (51-90)68 (56-73)67 (40-83)67.5 (40-90)
Smoker (%)61.7∗45.050.060.0∗23.5∗50.4
Statin user preop (%)48.950.050.040.029.4∗46.2
Statin user postop (%)59.163.263.360.041.2∗60.9
Diabetic (%)16.725.036.760.0∗22.227.9

∗p > 0.05.

Significant stenoses were assessed for feasibility of intervention by angiography regardless of symptomatology or ABPI. The type of intervention was at the discretion of the surgeon depending on the anatomy and location of the stenosis and included percutaneous angioplasty, surgical angioplasty, and repeat grafting.

Statistical Analysis 

Statistical analyses were performed with SAS, v9.1 (SAS Institute, Cary, NC), and with StatsDirect, v2.4.1 (StatsDirect). Patency, limb salvage, and survival rates were calculated with the life-table method. Patient demographics, procedure, and graft characteristics were compared for onset of significant lesions and occlusions using Pearson's product-moment correlation. p < 0.05 was taken as being significant.

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Results 

There were 12 deaths during the study period (6.1%). There were 118 grafts to the above-knee popliteal artery (55.6%), 63 to the below-knee popliteal artery (29.7%), and 31 to crural vessels (14.7%), which is comparable to other series.2 Six patients (3.0%) required lower limb amputation during the surveillance period. Two of these were during the original hospital admission, one was at 3 months, one was at 12 months, and the final one was before the 18-month surveillance scan. No femorocrural prosthetic grafts were performed during the study period.

Overall, 6.6% of grafts were performed for aneurysmal disease, 55.2% for disabling claudication, and 38.2% for critical ischemia (Table II).

Table II. Indications for surgery
Graft type
IndicationsAKVAKPBKVBKPFCV% of total grafts performed
Aneurysmal disease (%)3.87.514.80.00.06.6
Disabling claudication (%)56.465.051.922.254.855.2
Critical ischemia (%)39.827.533.377.845.238.2

Primary assisted patency rates of all grafts at 1, 6, and 18 months were 95.7%, 84.0%, and 71.3%, respectively, while the cumulative assisted primary patency for all grafts at 18 months was 78.4%. This was composed of 77.9% and 79.5% patency for venous and prosthetic bypasses, respectively. Patency rates were comparable between vein grafts in the above and below-knee positions, with 18-month patency of 86.0% and 79.5%, respectively. Forty-six grafts (21.6%) occluded during the program. The occlusion rate over the course of the surveillance period was 18.1% for femoropopliteal vein grafts, while prosthetic femoropopliteal grafts failed in 20.4% of cases. At the end of the 18-month follow-up period, the BKP group had the highest cumulative occlusion rate, with nearly half of grafts failing.

There were 26 occlusions (56.6%) preceded by a stenotic lesion on graft surveillance, while the remaining 20 (43.4%) occurred de novo, having had no previous stenotic lesion. De novo occlusions accounted for 95.9% and 66.5% of occlusions in the prosthetic and femorocrural grafts, respectively. Less than 3% of all femoropopliteal vein grafts developed an occlusion de novo, which accounted for 12.5% of all occlusions in this group. The temporal onset of occlusions is demonstrated in Figure 1.

Nonsignificant graft stenoses were common and had a variable natural history. While 58.3% of such lesions progressed and underwent revision, the remainder either resolved or failed to progress. Peak prevalence of significant lesions was at 6 months. However, the prevalence of significant lesions changed over the surveillance period. This variation was in part due to new onset of graft lesions, regression of existing lesions, occlusions, and interventions.

Throughout the study period, 56.2% of grafts remained stenosis-free. The prevalence of significant and nonsignificant stenosis in all grafts was 21.2% and 22.6%, respectively. This consisted of 23.9% and 25.2% among venous conduit and 12.2% and 10.2% among prosthetic conduit, respectively. Among the vein grafts, stenoses in the graft itself were common, but these tended to be moderate in severity and to have a high rate of resolution and a low rate of subsequent occlusion. There were also high rates of proximal anastomotic stenoses, with very few stenoses at the distal anastomosis even among the femorocrural group.

Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6 display the prevalence of stenoses and occlusions by graft, and Figure 7 demonstrates the prevalence by site.

Overall, 40 grafts required intervention (19.3%), 40.5% of which were carried out at 6 months (Fig. 8). Of interventions, 7.5% were in thrombosed grafts; the remainder were performed for a significant stenosis or inflow or outflow disease (see Table III). Figure 9 demonstrates the proportion of interventions according to graft type. Following intervention, 40% of grafts remained stenosis-free; 25% developed a recurrent stenosis at the intervention site, while 35% developed a new stenosis. Overall, a quarter of the grafts that required intervention subsequently underwent a second procedure for recurrent stenosis.

Table III. Location of significant stenosis requiring intervention
Location of significant stenosisNumber requiring intervention (% of total interventions)
Proximal anastomosis20 (50.0)
Graft3 (7.5)
Distal anastomosis9 (22.5)
Multiple levels6 (15.0)
Inflow1 (2.5)
Outflow1 (2.5)

As a group, vein grafts were more likely to develop a progressive stenosis prior to occlusion, with 21 of the 36 occlusions in this group predated by a stenotic lesion (58.3%). In the prosthetic grafts, only two of the 10 (20%) occlusions were documented to have a previous stenosis.

Significant stenoses within the prosthetic group were uncommon, usually developing after 6 months. These lesions were more likely to occur at the distal anastomosis but interestingly were poor predictors of occlusion.

Analysis with respect to age revealed an interesting trend. Patients under 60 and over 70 had a graft occlusion or significant stenosis in 54.1% and 53.3% of cases, respectively, compared to only 38.8% in the 61-70 age group, although this failed to reach statistical significance (p > 0.05).

Overall, graft occlusion was more prevalent in those not taking a statin postoperatively. In those not taking and those taking a statin, 32.6% and 22.8% of grafts occluded, respectively (p < 0.05). However, similar proportions of significant stenoses were seen in both those patients taking and those not taking statins. When individual grafts are considered, statin use was especially protective against occlusion and the development of significant stenoses in the AKV group (p < 0.05). No such benefit was seen in either prosthetic group. In the FCV grafts, there was a trend toward a better outcome with statin usage, where 22.8% of grafts occluded, compared to those not using statins postoperatively, where 32.6% of grafts failed.

Surprisingly, preoperative smoking status was predictive of neither the development of significant stenoses nor occlusion. There was a trend toward improved outcome in the above-knee grafts over the 18-month period, but this did not reach statistical significance (r = 0.18, p = 0.25).

The presence of hypertension, hypercholesterolemia, or diabetes was not predictive of poor outcome within the five groups.

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Discussion 

Early flow disturbances due to stenotic lesions have been associated with future graft failure.34 The majority of grafts with a stenosis ≥75% eventually occlude, making this the widely accepted threshold for intervention.29 Depending on the definition of a stenosis, previous studies document a 20-37% incidence of duplex-detectable flow disturbances after graft implantation,23, 31, 35 which was broadly similar to the numbers seen in our institution. This series includes all consecutive infrainguinal grafts, without subselection according to conduit type or distal target. The patency rates therefore fall somewhere between the traditionally favorable patency rates for autologous vein and unfavorable patency rates for below-knee or prosthetic grafts.

Few prospective, randomized trials have been carried out to assess the efficacy of graft surveillance. One of these studies demonstrated improved graft patency and limb salvage because of a duplex ultrasound program, while a second, more recent randomized trial was unable to show any such benefit.24, 26 During the first 6 months following vein graft bypass surgery, lesion onset and progression reach a plateau, with most of the lesions found during the first 6 months progressing over the next 6.36 In contrast, only a minority of grafts free of any significant stenoses at 6 months progress to occlusion.

Those who argue against surveillance cite the poor correlation of thrombosis with specific duplex scan parameters, given changes in inflow and outflow anatomy and hemodynamics in the graft over time. Protagonists point to the fact that 65% of those grafts that eventually occlude have an associated significant stenosis, while only 12% of the grafts that occlude have no prior evidence of stenosis.31 In addition, patency rates are improved following intervention in a failing or stenosed graft compared to those treated conservatively.10, 11, 12, 13, 37, 38, 39

In many cases bypass is performed for tissue loss and gangrene. Early patency often not only allows healing of ulcers and amputation sites but encourages the development of collaterals. This explains, in part, the phenomenon of an asymptomatic late graft occlusion even though the bypass was originally for critical disease. This is highlighted by reported series where extremities that can support bypass grafts for longer periods fare better, even if they eventually fail.1

A large number of stenoses were found, with almost twice as many among venous conduits than prosthetic grafts. This would not simply be explained by the additional stenoses related to remnant valve cusps. There also appeared to be a difference in distribution, with significant stenoses more commonly noted at the proximal anastomosis of infrainguinal vein grafts and distal lesions more commonly noted among prosthetic grafts. This probably represents a mismatch in the size of the vein compared to the artery since all grafts were reversed long saphenous vein. The increased compliance mismatch that occurs between prosthetic grafts, especially to small-diameter arteries, explains the higher numbers of distal lesions in the prosthetic group.7

Unfortunately, a small number of occlusions occurred in patients with significant lesions, often while awaiting intervention. This highlights the need for prompt action once a significant lesion is detected. Despite the intensive follow-up, the program failed to detect lesions prior to occlusion in a large percentage of prosthetic and femorocrural grafts, so perhaps these groups are poorly served by surveillance. These groups are probably at higher risk of failure because the femorocrural group has multilevel disease and the prosthetic group is more likely to have redo procedures. Of this large number of patients, in whom graft surveillance has a poor predictive value, only the femorocrural group had a significant contribution of progressive stenosis to occlusions. This explains the reluctance of some units to include prosthetic conduit in their surveillance programs and the preference of anticoagulants to antiplatelet agents in this group. The dismal outcomes of occlusion in prosthetic and crural grafts may justify their intensive follow-up, despite the low yield.

It was surprising to find that smoking cessation conferred little overall benefit in terms of patency. This could possibly be due to smoking having continuing adverse effects after 18 months or the traditional poor correlation between patients' stated and actual habits.38, 39, 40 Improved outcome in patients on statins has been recently reported,41, 42 but these studies concentrated on long-term statin therapy. It was interesting that on subgroup analysis it was at the 1-month time point that statin therapy showed most benefit, suggesting a role for statins in the immediate postoperative period. The potential mode of action for this improved patency is hard to explain but may be related to the anti-inflammatory action of statins and their antiproliferative action in reducing neointima formation.43

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Conclusion 

Our findings suggest that graft surveillance is a valid method for detecting the presence of significant lesions at high risk of failure without intervention in the AKV and BKV groups. The case for surveillance was not as strong in the FCV group. Surveillance for prosthetic grafts generates a low yield and detects significant stenoses prior to occlusion in very few cases. Statin therapy was protective against graft failure, particularly in the early postoperative period.

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The authors thank Renovo plc and the Vascular Laboratory at Manchester Royal Infirmary for their assistance in producing this work.

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References 

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PII: S0890-5096(07)00284-1

doi:10.1016/j.avsg.2007.07.019

Annals of Vascular Surgery
Volume 21, Issue 6 , Pages 695-703, November 2007

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