Volume 37, Issue 1, Pages 47-53 (January 2003)

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ABSTRACT

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Modifiable patient factors are associated with reverse vein graft occlusion in the era of duplex scan surveillance☆☆☆★★★

Presented at the Fiftieth Annual Meeting of the American Association for Vascular Surgery, Boston, Mass, Jun 9-12, 2002.

Received 17 June 2002; accepted 19 August 2002.

Abstract

Objective: Modifiable patient factors that contribute to graft occlusion may be addressed after surgery. To determine risk factors associated with reverse vein graft (RVG) occlusion, we examined the characteristics and duplex scan surveillance (DS) patterns of patients with RVGs. Methods: Patients treated with RVG from January 1996 through December 2000 were identified from a prospective registry. The study population consisted of all patients with RVGs performed during the study period with grafts that subsequently occluded. Patients whose grafts remained patent served as age-matched and gender-matched control subjects. The prescribed DS regimen was every 3 months for the first postoperative year and every 6 months thereafter. Early DS failure was defined as having no DS within the first 3 months. Cox proportional hazards analysis was used to compare the two groups. Hazard ratios were calculated. Results: During the study period, 674 patients underwent RVG. Fifty-five patients with occluded RVGs were compared with 118 with patent RVGs. The follow-up period for occluded grafts was 13.40 ± 12.59 months and for patent grafts was 32.40 ± 15.61 months. Dialysis therapy, a known hypercoagulable state, continued smoking, and DS failure were independent factors associated with RVG occlusion. The hazards ratio for dialysis was 6.45 (95% CI, 3.07 to 13.51; P < .001), for current smoking was 4.72 (95% CI, 2.5 to 8.85; P < .001), for hypercoagulable state was 2.99 (95% CI, 1.47 to 6.10; P = .003), and for early DS failure was 2.43 (95% CI, 1.29 to 4.59; P = .006). Conclusion: Continued smoking and failure to undergo DS within the first three postoperative months are modifiable factors associated with RVG occlusion. Smoking cessation and graft surveillance must be stressed to optimize patency of infrainguinal RVGs. (J Vasc Surg 2003;37:47-53.)

Article Outline

• Abstract

• Methods

• Patient characteristics

• Statistical analysis

• Results

• Patient characteristics

• Factors associated with graft occlusion during follow-up period

• Effect of independent risk factors on graft patency

• Factors associated with noncompliance

• Discussion

• References

• Copyright

Infrainguinal bypass graft occlusion occurs in 10% to 30% of grafts.1, 2, 3, 4, 5 As the population ages, the number of infrainguinal reconstructions continues to increase. Therefore, all surgeons performing reconstruction for limb ischemia will encounter more patients needing and having had leg bypass grafts. The patency rate for repeat leg bypass grafting ranges from 20% to 57% at 5 years.6, 7, 8, 9 The amputation rate after reverse vein graft (RVG) occlusion is 10%.10 In our experience, revision of stenosis detected with duplex scan results in a 5-year assisted primary patency rate of 92%.11 The importance of detection and correction of graft-threatening lesions to prevent graft occlusion is therefore obvious.2, 11, 12

Data strongly suggest that routine duplex scan surveillance (DS) and correction of stenosis throughout the postoperative period improve graft patency.4, 11, 12, 13 Vein graft stenosis often precedes graft occlusion. Routine DS can effectively detect these lesions before occlusion. Sixty-nine percent of vein graft abnormalities are detected in the first 6 months, but abnormalities can develop at any time during the postoperative period.14 Therefore, the policy at our institution has been continued DS for the life of the graft. Postoperative DS and revision of detected lesions has been shown to be cost effective when compared with the treatment of graft occlusion.15, 16

Multiple reports have examined the various factors that affect the outcome of infrainguinal bypass grafts. These reports have largely focused on anatomic considerations, end-stage renal disease, hypercoagulable states, gender, choice of conduit, and diabetes mellitus.17, 18, 19, 20, 21 The goal of this report was to determine the causes of RVG occlusion that can be addressed during the postoperative period, specifically factors that are within patient and physician control.

Methods

Patient characteristics

Patients treated with infrainguinal RVG from January 1996 through December 2000 at Oregon Health & Science University and the Portland Veterans Affairs Medical Center were identified from prospectively maintained registries. Patients who underwent RVG during the study period with grafts that later occluded constituted the study group. An age-matched and gender-matched control group twice the size of the study group with grafts that remained patent was chosen. Data abstracted from the medical record included smoking status, medical history, DS pattern, time to graft occlusion, operative indication, previous ipsilateral leg bypass, previous inflow procedure, previous graft revision, type of vein graft, site of distal anastomosis, and survival. Patients were excluded if no follow-up information was available or if the RVG occluded before hospital discharge. If a patient had multiple RVGs, only the first graft was considered.

Survival data were obtained from the medical record when available or the Social Security Death Index website.22 Information from the Social Security Death Index website was considered valid if there was an exact match of first and last name and social security number.

The prescribed postoperative DS regimen was every 3 months for the first year, with the initial DS examination completed before hospital discharge and every 6 months thereafter. Early DS failure was defined as no DS within the first 3 months. Patients with graft occlusion before the first scheduled duplex scan examination were not considered to have DS failures. Late DS failure was defined as patients who underwent DS within the first 3 months but then failed to have DS from 6 to 12 months in the first postoperative year.

Current smoking was considered any cigarette smoking during the postoperative period. A patient was considered to have a hypercoagulable state if there was a documented diagnosis of antiphospholipid antibody, factor V Leiden, prothrombin gene mutation, antithrombin III deficiency, or protein C or S deficiency in the medical record. Only patients with more than one episode of graft thrombosis were routinely tested for a hypercoagulable state. All patients with a documented hypercoagulable state were treated with warfarin, except one patient who had a heterozygote factor V Leiden and had repeated gastrointestinal bleeding.

Criteria for patency and occlusion were those suggested by Rutherford et al.23 Graft occlusion was detected with physical examination or DS or both and then confirmed with angiography.

Statistical analysis

A Cox proportional hazards model was used to compare patients with occluded grafts with those with patent grafts. The variables included in the model were known risk factors for graft occlusion and the progression of arteriosclerosis (Table I). Hazard ratios for graft occlusion with 95% CIs were calculated for each variable. To compare the effects of the patient factors on patency, adjusted patency curves were calculated with the Cox regression model. These curves were statistically adjusted to control for the covariates in the model (Table I) and isolate the effect of the desired variable on graft patency. These curves are not univariate life-tables but are a form of multivariate analysis.

Table I.

Factors analyzed in Cox proportional hazards model


	Variable
	Age
	Rest pain or ulceration
	Gender
	Aspirin therapy
	Current smoking
	Known hypercoagulable state
	Diabetes
	Atrial fibrillation
	Hyperlipidemia
	Dialysis
	Prior inflow procedure
	Hypertension
	Late DS failure
	Early DS failure
	Prior revision
	Previous ipsilateral bypass
	Below-knee graft
	Saphenous vein graft
	Arm vein graft

Spearman correlation coefficients were calculated to evaluate the association between early DS failure and other markers of noncompliance. The markers of noncompliance used were failure to attend regular clinic appointments or failure to adhere to the prescribed DS regimen throughout the follow-up period. Correlation coefficients were also calculated for other patient factors, such as medical comorbidities and distance from the institution, which were hypothesized to have an association with noncompliance.

Results

Patient characteristics

From January 1996 to December 2000, 674 patients underwent RVG. Fifty-five patients, 20% of whose grafts had been revised before occlusion (n = 11), had a graft occlusion and constituted the study group. One hundred eighteen patients, 31% of whose grafts had been revised during the follow-up period (n = 36), matched for age and gender with patent grafts served as controls. The patient characteristics are listed in Table II.

Table II.

Characteristics of patients with occluded grafts (study group) compared with patients with patent grafts (control group)


Patient characteristics	Occluded grafts	Patent grafts	P value*
Mean age (y)	67.4	67.3	.95
Male gender	84% (46)	93% (110)	.3
Rest pain or ulceration	96% (53)	94% (111)	.5
Prior ipsilateral bypass	24% (13)	19% (22)	.3
Below-knee anastomosis	93% (51)	88% (104)	.3
Prior revision	20% (11)	31% (37)	.1
Current smoking	60% (33)	30% (35)	<.001
Aspirin therapy	78% (43)	77% (91)	.88
Known hypercoagulable state	18% (10)	8% (9)	.04
Diabetes mellitus	55% (30)	53% (63)	.81
Atrial fibrillation	18% (10)	19% (22)	.84
Dialysis therapy	18% (10)	3% (4)	.001
Warfarin therapy	44% (24)	27% (32)	.04
Hyperlipidemia	40% (22)	36% (42)	.58
Prior inflow procedure	47% (26)	37% (44)	.22
Hypertension	89% (49)	81% (96)	.17
Early DS failure	25% (14)	11% (13)	.01
Arm vein	15% (8)	5% (6)	.07
Late DS failure	20% (11)	14% (17)	.31
*P value calculated with independent sample two-tailed t test.

Factors associated with graft occlusion during follow-up period

The factors evaluated in the model that were not significantly associated with graft occlusion included hypertension, diabetes, atrial fibrillation, hyperlipidemia, aspirin therapy, prior ipsilateral leg bypass or inflow procedure, operative indication, below-knee distal anastomosis, late DS failure, and use of arm vein (data not shown). Prior graft revision was associated with a decreased risk of occlusion (hazards ratio, 0.55; P = .09). Dialysis therapy, continued smoking, presence of a known hypercoagulable state, and early DS failure were significant independent risk factors for graft occlusion. The hazard ratios of those factors associated with occlusion are listed in Table III.

Table III.

Hazards ratios for graft occlusion calculated with Cox proportional hazards model


Patient factor	No. of patients	Hazards ratio	95% CI	P value
Dialysis	14	6.45	3.07-13.51	<.001
Current smoking	68	4.72	2.50-8.85	<.001
Known hypercoagulable state	19	2.99	1.47-6.10	.003
Early DS failure	27	2.43	1.29-4.59	.006
Revision	47	0.55	0.27-1.09	.088

Effect of independent risk factors on graft patency

The mean time to occlusion was 13.4 ± 12.6 months (n = 55). The mean follow-up period for patent grafts was 32.4 ± 15.6 months (n = 118). With the Cox regression model, the effect of the independent variables on time to occlusion was evaluated. The adjusted patency curves are shown in Figs 1 to 4.

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Fig. 1. Adjusted assisted primary patency curve of RVGs comparing patients currently smoking (n = 68) with nonsmoking patients (n = 105). Curve was generated with Cox proportional hazard model. P < .001.

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Fig. 2. Adjusted assisted primary patency curve of RVGs comparing patients who fail early DS (n = 27) with compliant patients (n = 146). Curve was generated with Cox proportional hazard model. P = .006.

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Fig. 3. Adjusted assisted primary patency curve of RVGs comparing patients with end-stage renal disease (n = 14) with patients with normal renal function (n = 159). Curve was generated with Cox proportional hazard model. P < .001.

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Fig. 4. Adjusted assisted primary patency curve of RVGs comparing patients with known hypercoagulable state (n = 19) with patients without known hypercoagulable state (n = 154). Curve was generated with Cox proportional hazard model. P = .003.

Assisted primary patency rates were significantly lower for patients currently smoking than nonsmoking, for those on dialysis therapy compared with no dialysis, for those with early DS failure compared with compliant DS, and for those with a known hypercoagulable state compared with those without a known hypercoagulable state.

Factors associated with noncompliance

Early DS failure was associated with failure to comply with regular clinic visits and regular DS examinations throughout the duration of the postoperative period. No association was seen between these markers of compliance and cigarette smoking, driving distance to the institution, diabetes mellitus, prior ipsilateral bypass, dialysis, gender, or age. The correlation coefficients are listed in Table IV.

Table IV.

Association between early DS failure and compliance, comorbidities, and driving distance


Factor	Correlation coefficient*	P value;†
Failing regular visits	0.276	<.001
Current smoking	0.092	.23
Dialysis therapy	0.011	.89
Diabetes mellitus	−0.020	.79
Female gender	0.137	.07
Age	0.086	.26
Prior ipsilateral bypass	0.058	.45
Distance from institution	0.061	.43
*Spearman ρ correlation coefficients. †P value generated with two-tailed test of significance.

Discussion

The goal of this report was to identify patient factors that contribute to RVG occlusion that can be addressed and potentially modified during the postoperative period. In this group of patients, continued smoking and failure to participate in DS during the first 3 postoperative months were identified as modifiable patient factors associated with RVG occlusion.

Failure to undergo early DS was associated with an increased risk of graft occlusion. The logical assumption is that early DS detects graft-threatening lesions that are then revised, thus preventing graft occlusion. In this report, patients who had undergone graft revision were half as likely to have an occlusion during the follow-up period as patients without revision (P = .09). Although this did not reach statistical significance, the trend was strong. Probably this represents a statistical type II error resulting from a small sample size (n = 47 revisions). It has been established at this institution and others that detection of stenosis with DS and subsequent revision improves graft patency.4, 11, 13, 14

Early DS failure was an independent risk factor associated with graft occlusion; however, late DS failure was not significantly associated with occlusion in patients participating in early DS. Other authors have suggested that almost all vein graft lesions are detectable in the early postoperative period and that less intensive surveillance may be justified if early studies do not reveal an abnormality.24, 25 Previous studies from our institution have found that 69% of stenoses detected and subsequently revised are detected in the first 6 months and 17% are detected from 9 to 12 months.13

Routine DS can only improve patency if patients are compliant with the prescribed regimen. In this report, an association was found between early DS failure and failure to participate in regular follow-up for the duration of the postoperative period. Because a significant correlation was seen between early DS failure and failure to participate in regular follow-up, we can conclude that early DS failure is a marker for poor compliance throughout the postoperative period. This association potentially explains the decreased RVG patency out to 48 months.

Failure to undergo DS in the first 3 postoperative months is a combination of system and patient failure. The results of this study confirm the importance of early DS examinations. Other investigators have found that intraoperative duplex scan and revision reduces early graft failure.26 Ten percent of the RVGs were immediately revised on the basis of abnormal intraoperative DS findings. Intraoperative DS after RVG would reduce the incidence rate of early DS failure. However, to date, this has not been done at our institution.

One hypothesis was that older patients with multiple medical problems would be less likely to participate in routine follow-up. In this series, failure to participate in routine follow-up was independent of patient comorbidities. No significant association was seen between failure of 3-month DS and cigarette smoking, dialysis, prior ipsilateral bypass, diabetes mellitus, gender, driving distance to the hospital, or age. In this study, these issues did not influence a patient's ability to participate in routine follow-up or DS. Other issues that might influence patient compliance with follow-up are terminal illness, cultural barriers, or lack of transportation to the clinic. These issues are beyond the scope of this analysis but should be evaluated in future studies.

The association between decreased graft patency and cigarette smoking has been previously established.27, 28 Greenhalgh et al27 prospectively followed patients with aortoiliac reconstruction and RVG and serially measured serum markers for tobacco use. The patients with occluded grafts had significantly elevated blood levels of carboxyhemoglobin. Similarly, Wiseman et al28 measured serum smoking markers in patients with occluded and patent vein grafts. These authors found that the patients with occluded grafts had significantly elevated levels of smoking markers compared with those with patent grafts. Patency was significantly higher in nonsmoking patients when compared with patients who smoked (84% versus 63%; P < .02). Other investigators have shown an association between cigarette smoking and the development of graft stenosis.29 In our report, continued smoking had a profound effect on graft patency. This information shows the importance of continued patient education about smoking cessation.

The use of aspirin was not associated with a decreased risk of graft occlusion in the regression model. Multiple previous studies, including two metaanalyses, have shown that antiplatelet therapy reduces the incidence rate of graft occlusion.30, 31 However, most patients in this report were taking aspirin. Most of those not using aspirin were taking warfarin, which was initiated for a prior graft occlusion, hypercoagulable state, or atrial fibrillation. Because such a large percentage of the patients in both groups were taking aspirin or were undergoing anticoagulation, a larger sample size would be necessary to show an independent effect of aspirin on graft patency.

In conclusion, this study emphasizes the importance of routine DS and smoking cessation. Patients with failure for early DS and who continue to smoke cigarettes are more likely to have graft occlusion. Smoking cessation and adherence to postoperative DS must be stressed to optimize graft patency.

Discussion

Dr Alun H. Davies (London, United Kingdom). Can I ask you two questions? One, you have presented us with patency data, but surely the main aim of surveillance is actually with respect to limb salvage. So, do you have any data on your limb salvage rather than patency rates, is my first question.

And the second question is, you have started your surveillance program at 3 months, whereas several other people would believe in actually starting it at 1 week, 6 sweeks, and then 3 months.

Dr Mary E. Giswold. To address the first question, we did not look at limb salvage in this paper. So, although it is a good question, I do not have that information.

Initally, from 1996 to 1997, patients did not routinely undergo duplex prior to discharge. The current duplex surveillance policy at Oregon Health & Sciences consists of a duplex exam prior to discharge from the hospital, every 3 months for the first postoperative year, and then every 6 months thereafter. The results of this study demonstrate the importance of early duplex surveillance.

Dr George Andros (Los Angeles, Calif). You defined these variables as modifiable, but are they really? Perhaps in the next 2 years you will institute an education program to modify these variables and teach patients to attend the clinic and not to smoke. At that time, maybe you will let us know how well education serves to modify adverse variables.

Dr Giswold. In the vascular clinic at OHSU, smoking cessation is discussed at every visit. Patients are reminded in a constructive supportive manner about the importance of smoking cessation. We also routinely discuss aspirin therapy and compliance with duplex surveillance. These discussions are documented in the clinic note for each visit.

Dr Thomas Holzenbein (Vienna, Austria). One of your modifiable risk factors was aspirin therapy. How do you monitor aspirin therapy? Or did you use Coumadin in any of these patients?

Dr Giswold. About 80% of the patients were on aspirin. This is based on information available in the clinic chart. Most of the patients that were not on aspirin were actually on Coumadin for either atrial fibrillation or a hypercoagulable state.

Dr Mark Nehler (Denver, Colo). The take-home message of your paper is that noncompliant patients get poor results for graft surveillance. We have actually used this as criteria, not in isolation, but with other factors—substantial foot necrosis and/or alternate conduit. To not offer limb salvage attempts in historically noncompliant patients because if they do not comply with the graft surveillance program limb salvage is often not going to be successful. Do you have any comment?

Dr Giswold. At OHSU, we do not consider socioeconomic status when operating for limb salvage. When this situation does arise, compliance can be optimized by duplexing the graft prior to the patient's discharge from the hospital.

Dr William D. Turnipseed (Madison, Wis). I am interested in looking at the 55 graft failures and the time interval at which they occurred. Did they all occur within that 3-month or 6-month period between failed visits? Are you culling out the technical errors to begin with, or do you think patient compliance alone is an important factor in keeping these grafts open?

Dr Giswold. The mean time to graft occlusion was 13 months. The mean time to occlusion for the patients who failed to have a duplex exam in the first 3 months was 8 months. Patients with grafts that occluded prior to discharge were excluded. Therefore, many of the patients whose grafts occluded because of a technical error were excluded. So, I think that the effect of the duplex exam and then having a subsequent revision is real.

Dr G. Patrick Clagett (Dallas, Tex). Would you care to speculate on the mechanism of occlusion among the smokers? It would seem to me that you might have some information with regard to whether they more prone to intimal hyperplastic events, or is it perhaps some ill-defined hypercoagulable influence that leads to occlusion among smokers?

Dr Giswold. The time to occlusion for the patients smoking cigarettes was 14 ± 12 months. The time to occlusion for patients who were not smoking was 31 ± 16 months. This was significantly different, with a P value of less than .001. This difference could be attributed to accelerated neointimal hyperplasia or arteriosclerosis. There were more patients who occluded sooner in the group of patients who continued smoking; potentially these patients had a degree of hypercoagulability related to smoking.

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Portland, Ore

From the Division of Vascular Surgery, Oregon Health & Science University; and the Veterans Affairs Medical Center

☆ Supported in part by grant # R01HL45267 NIH, NHLBI.

☆☆ Competition of interest: nil.

★ Reprint requests: Gregory L. Moneta, MD, Professor and Chief, Division of Vascular Surgery, Oregon Health & Science University, 3181 SW Sam Jackson Park Rd OP-11, Portland, OR 97201-3098.

★★ 0741-5214/2003/$30.00 + 0

PII: S0741-5214(02)75145-8

doi:10.1067/mva.2003.4

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