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Ann Thorac Surg 2008;85:520-524. doi:10.1016/j.athoracsur.2007.10.061
© 2008 The Society of Thoracic Surgeons
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Original Articles: Cardiovascular

Impact of Saphenous Vein Graft Radiographic Markers on Clinical Events and Angiographic Parameters

Stephen A. Olenchock, Jr, DOa, Dimitri Karmpaliotis, MDb, William J. Gibsonc, Sabina A. Murphy, MPHd, Matthew C. Southard, BSd, Lauren Ciaglo, BSd, Jacqueline Buros, BSd, Michael J. Mack, MDe, John H. Alexander, MDf, Robert A. Harrington, MDf, Robert M. Califf, MDf, Nicholas T. Kouchoukos, MDg, T. Bruce Ferguson, Jr, MDh, C. Michael Gibson, MS, MDd,*

a Cardiothoracic Surgery Department, Tufts University School of Medicine and Caritas St. Elizabeth’s Medical Center, Boston, Massachusetts
b The Fuqua Heart Center, Piedmont Hospital, Atlanta, Georgia
c Massachusetts Institute of Technology, Cambridge, Massachusetts
d Cardiovascular Divisions, Departments of Medicine, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts
e Cardiopulmonary Research, Science and Technology Institute, Dallas, Texas
f Duke Clinical Research Institute, Durham, North Carolina
g Missouri Baptist Medical Center, St. Louis, Missouri
h East Carolina Heart Institute, Brody School of Medicine at East Carolina University, Greenville, North Carolina

Accepted for publication October 17, 2007.

* Address correspondence to Dr Gibson, TIMI Data Coordinating Center, 350 Longwood Avenue, First Floor, Boston, MA 02115 (Email: mgibson{at}perfuse.org).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: Use of saphenous vein graft (SVG) radiographic markers has been associated with shorter cardiac catheterization procedure times and reduced contrast agent volume for postoperative coronary artery bypass graft (CABG) catheterizations. Use of such markers is varied and often operator-dependent, as the effect of SVG markers has not been fully evaluated. The goal of the present analysis was to evaluate the association of SVG markers with clinical outcomes and graft patency.

Methods: Data were drawn from the Project of Ex-vivo Vein Graft Engineering via Transfection (PREVENT) IV trial of patients undergoing CABG at 107 hospitals across the United States. Repeat angiography was performed within 12 to 18 months after CABG. The SVG markers were used at the discretion of the surgeon and were identified on the follow-up angiogram as any device used to mark the ostium, regardless of shape.

Results: The SVG markers were present in 51.2% of evaluable patients (910 of 1,778) and 52.3% of SVGs (2,228 of 4,240). Among patients with totally occluded SVGs (n = 911), visual identification of the SVG was obtained more frequently in those with an SVG marker (90.7% vs 72.1%, p < 0.001). The SVG stenosis 70% or greater at follow-up did not differ by use of markers (25.8% with marker vs 24.4% without marker, p = not significant). These findings were also consistent in ostial lesions (n = 942). Long-term death or myocardial infarction (MI) was similar by use of marker. The perioperative CABG MI was higher in patients with SVG markers (10.1% vs 5.5%, odds ratio adjusted 1.86, p = 0.021).

Conclusions: Saphenous vein graft radiographic markers were associated with higher rates of direct visualization of totally occluded SVGs without an adverse effect on graft patency or long-term clinical outcomes, but the association of SVG markers with increased perioperative CABG MI warrants further examination.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Use of saphenous vein graft (SVG) radiographic markers has been associated with shorter cardiac catheterization procedure times as well as a reduced volume of contrast agent for postoperative coronary artery bypass graft (CABG) catheterizations [1, 2]. It has been demonstrated that shorter catheterization times benefit the patient through reduced exposure to fluoroscopy-related radiation as well as the avoidance of overexposure to potentially toxic contrast agents [1, 3–6]. Use of such markers is varied and often operator-dependent [7] as the effect of SVG markers on clinical outcomes and subsequent graft patency has not been fully evaluated. Additionally, the association of SVG radiographic markers with postoperative complications and long-term survival is not well-characterized.

Given the uncertainty of the relationship of SVG radiographic markers with clinical outcomes and subsequent graft patency, the present analysis sought to evaluate the association of use of SVG markers with intermediate-term graft patency and angiographic outcomes at 12 to 18 months postsurgery, as well as postoperative and long-term clinical morbidity and mortality.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Patient Population
Data were drawn from the Project of Ex-vivo Vein Graft Engineering via Transfection (PREVENT) IV trial, the design of which has been described in detail elsewhere [8, 9]. In brief, the PREVENT IV trial was a phase III, multicenter, randomized, double-blind, placebo-controlled trial in which autologous vein grafts were treated ex vivo with edifoligide for patients undergoing primary CABG surgery (n = 3,014). Patients, age 18 to 80 years old, undergoing a first, isolated CABG surgery for atherosclerotic coronary artery disease with at least two planned vein grafts, were eligible. For the purpose of eligibility, grafts with multiple distal anastomoses were counted as single grafts. The first 2,400 patients enrolled were assigned to an angiography cohort and scheduled to return for angiography 12 to 18 months after surgery. Institutional Review Board approval was obtained at all sites and all patients gave written informed consent prior to participation. The present analysis includes the 1,778 patients who were assigned to the angiography cohort, who survived to 12 to 18 months, and who underwent the protocol angiography.

Each patient’s harvested vein was treated ex vivo with either edifoligide, formulated as double-stranded oligonucleotide at a concentration of 40 µmol/L or 0.38 mg/mL, or an identical appearing buffered normal saline placebo. The study drug was administered using a pressure-mediated delivery system (Corgentech Inc, South San Francisco, CA); a trough inserted in a fluorinated ethylene polypropylene tube attached to a pressure syringe. The vein was harvested in the usual manner, placed on the trough, and inserted into the tube which was then filled with either edifoligide or placebo solution. Six pounds per square inch of nondistending pressure was applied to the tube for 10 minutes. The treated vein was then removed from the device, divided into appropriate lengths for grafting, and grafted into the patient using standard surgical techniques. Other than administration of the study drug, all graft handling, surgical, and medical interventions were left to the discretion of the operating surgeon, including the use of SVG markers.

Angiographic Evaluation
The SVG radiographic markers were identified on the follow-up angiogram as any device used to mark the ostium, regardless of shape. In the absence of visualization on the angiogram, total occlusions were assessed by aortogram study, retrograde filling at the distal anastomosis, lack of competitive flow, or clinical documentation. Number and location of SVGs placed during surgery was known by the angiographic core laboratory, so all SVGs were accounted for on the follow-up angiogram during the assessment of patency and percent stenosis.

The primary endpoint of the PREVENT IV trial was vein graft failure (≥75% vein graft stenosis) occurring 12 to 18 months after CABG surgery. Percent stenosis was measured by quantitative coronary angiography. Other angiographic endpoints included the thrombolysis in myocardial infarction (TIMI) frame count [10, 11] and the TIMI myocardial perfusion grade [12]. All angiograms were interpreted at the PERFUSE Angiographic Core Laboratory in Boston, MA.

Patients were contacted at 6 and 9 months and at 1 year after surgery for assessment of clinical events. Annual follow-up is ongoing and planned at 2, 3, 4, and 5 years. Median follow-up at the time of the present analysis was 3.1 years (interquartile range [IQR] 3.1 to 4.0 years). All suspected MIs and revascularization procedures were adjudicated by a blinded, independent clinical events committee using prespecified criteria. Perioperative index CABG MI was defined as a creatine kinase (CK) MB fraction equal to or greater than 10 times the upper limit of normal (ULN) or equal to or greater than 5 times the ULN with new greater than 30-millisecond Q waves in two contiguous leads; or, if postoperative CK-MB samples were not available, new, greater than 30-millisecond Q waves in two contiguous leads. Perioperative index CABG MI was diagnosed if CK-MB was elevated within 24 hours of surgery, without an interval clinical event, and not attributable to a preoperative MI.

Statistical Analysis
Clinical and angiographic characteristics were summarized in terms of frequencies and percentages for categoric variables, and by median, 25th, and 75th percentiles for continuous variables. Differences were assessed using the {chi}2 test for categoric variables and the Wilcoxon rank sum test for continuous variables. The association of graft failure and marker use was evaluated using a logistic regression model, clustering for enrolling site. Long-term clinical endpoints of death, death or MI, and need for repeat revascularization were assessed with the log-rank test. Cumulative event rates were calculated by the Kaplan-Meier method, with time to the first event as the outcome variable.

A multivariable model for perioperative CABG MI was developed using a stepwise backward selection model, clustered on enrolling site. Candidate variables included baseline and surgical characteristics that differed between patients with and without a perioperative CABG MI on univariate analysis at the p less than 0.25 thresholds, including gender, weight, ejection fraction, need for urgent surgery, use of cardiopulmonary bypass, duration of surgery, hypercholesterolemia, prior percutaneous coronary intervention (PCI), and cerebrovascular disease. Variables retained in the model were weight, ejection fraction, cerebrovascular disease, prior PCI, and hypercholesterolemia; SVG radiographic marker use was also included in the final model. All statistical analyses were performed using Stata/SE, version 9.0 (StataCorp, College Station, TX).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Repeat angiography was performed in 1,829 patients enrolled at 100 hospitals, of whom an evaluation on markers was possible in 97% of patients (n = 1,778). Median time from surgery to repeat angiography was 13 months (IQR 12 to 14 months). The SVG radiographic markers were present in 51.2% of evaluable patients (910 of 1,778) and 52.3% of SVGs (2,228 of 4,240). Use of markers was correlated within sites (n = 100 sites), with 38% of sites using markers in 10% or less of patients and 36% using markers in 90% or greater of patients. Patients who received SVG radiographic markers were more likely to have been in New York Heart Association (NYHA) class I at baseline, more likely to have undergone urgent bypass surgery, and more likely to be smokers (Table 1). Duration of surgery was approximately 7 minutes longer in patients in whom SVG radiographic markers were used (Table 1).


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  		Table 1 Baseline and Surgical Characteristics by Use of Saphenous Vein Graft Radiographic Markers
 
SVG Markers and Angiographic Follow-Up
Among patients with totally occluded SVGs (stenosis 100%; n = 911), the visual identification of the SVG was obtained more frequently in those with an SVG marker than those without an SVG marker (90.7% vs 72.1%, p < 0.001; Fig 1). Among those without visualization of the graft, method of assessment of patency is shown in Table 2.


Figure 1
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  		Fig 1. Visual identification of totally occluded saphenous vein grafts (SVGs) at 12 to 18 months post-coronary artery bypass grafting by use of radiographic markers.

 

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  		Table 2 Assessment of Total Occlusion Criteria in the Absence of Visualization of Saphenous Vein Grafts (SVG) a
 
The SVG stenosis at angiographic follow-up did not differ by use of markers, with a stenosis 30% or less in 48.0% of SVGs with a marker versus 50.1% of SVGs without a marker, and stenosis of 70% or greater in 25.8% of SVGs with a marker versus 24.4% of SVGs without a marker (Fig 2; p = 0.37). Likewise, the occurrence of total occlusion was not different by marker use (22.2% in patients with SVG marker versus 20.9% in patients without SVG markers, p = 0.29). The 942 lesions that were located in the ostium had a much higher percent stenosis overall (84% had stenosis ≥70%), but even among these ostial lesions there was no difference between the frequency of stenosis 70% or greater when an SVG marker was used compared with when no SVG marker was used (85.0% vs 83.5%, p = 0.51); conversely, a stenosis of 30% to 70% was present in 15% of patients with an SVG marker and an ostial lesion compared with 16.6% of patients without an SVG marker but with an ostial lesion. Results were consistent within each of the randomized treatment arm groups (stenosis ≥70% in edifoligide group, 25.5% with SVG markers vs 24.1% without SVG markers, p = 0.48; stenosis ≥70% in placebo group, 26.2% with SVG markers vs 24.6% without SVG markers, p = 0.40; p-interaction = 0.926).


Figure 2
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  		Fig 2. Saphenous vein graph (SVG) stenosis within 18 months by use of SVG radiographic markers. (NS = not significant.)

 
There was also no difference by use of SVG markers in flow in the SVG (TIMI frame count median 25 (IQR 18.8 to 33.1) for those with markers and median 25 (IQR 17.5 to 33.8) for those without markers (p = 0.27), or presence of myocardial perfusion (77% for those with and 79% for those without markers, p = 0.24).

SVG Markers and Clinical Outcomes
The need for an intraaortic balloon pump (IABP) did not differ among those with versus without SVG radiographic markers (Table 3). Perioperative index CABG MI occurred significantly more frequently in patients with SVG markers (10.1% vs 5.5%, p < 0.001). In a multivariable logistic model adjusting for correlates of perioperative index CABG MI (weight, ejection fraction, cerebrovascular disease, prior PCI, and hypercholesterolemia) and enrolling site, use of SVG markers remained associated with an increase in perioperative CABG MI (odds ratio 1.86, 95% confidence interval [CI] 1.10 to 3.16, p = 0.021). There was no difference in long-term mortality, MI, or need for repeat revascularization (Table 3).


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  		Table 3 Clinical Outcomes by Use of Saphenous Vein Graph Radiographic Markers
 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
Use of SVG radiographic markers was not associated with an adverse effect on graft percent stenosis in a serial evaluation of more than 4,000 SVGs at 12 to 18 month postsurgery, but was associated with a higher rate of ascertainment of SVG patency on angiography. While there was no impact on long-term death or MI through a median of three year follow-up, perioperative CABG MI occurred nearly twice as frequently in patients with SVG radiographic markers, a finding that remained after adjustment for confounders such as longer surgery duration and more urgent CABG in a multivariable model.

Postoperative CABG angiography can be challenging, particularly when surgical notes and (or) earlier catheterizations are not available for comparative anatomy. This may be especially true in the setting of urgent catheterization due to myocardial infarction, when both time and completeness of revascularization are of particular importance. Higher volumes of contrast can increase the risk for contrast-induced nephrotoxicity and other complications [13]. Prior studies have demonstrated that use of SVG markers reduced fluoroscopy times by approximately 23% to 30% and reduced contrast volume by approximately 12% to 20% in the setting of postoperative CABG catheterizations [1, 2]. The decision to use SVG markers tended to be an "all or none" phenomenon that was specific to the individual surgeon-site, with 38% of sites using markers in 10% or less of patients and 36% using markers in 90% or greater of patients; only in one-quarter of the sites did the frequency of use vary between 10% and 90% of patients.

A prior retrospective analysis by Eisenhauer and colleagues [14] evaluated graft patency in 716 SVGs (n = 335 patients) from a single center, with time from CABG to angiography ranging from less than 1 year (n = 138) to greater than 15 years (n = 27). The study found no difference in SVG patency in late-term angiography of greater than 5 years post-CABG, but angiography performed within 5 years of surgery actually demonstrated higher patency associated with SVG marker use (90.0% vs 46.9% if <1 year postoperative CABG, n = 138; 80.0% vs 59.7% if >1 to 5 years postoperative CABG, n = 157). Based on these findings, the authors suggested marker ring use may improve patency, although no subsequent data have supported this hypothesis and the number of SVGs in the study was relatively small.

Conversely, it is possible that placement of the marker could have resulted in inflammation, smooth muscle proliferation and migration, or deposition of extracellular matrix, all known to cause intimal hyperplasia and subsequent vein graft failure [15]. Despite this, no difference was observed in graft failure on the angiogram in the present study. While it is possible that markers may have resulted in inflammation or smooth muscle proliferation, the amount of such changes may not have been large enough to induce the degree of intimal hyperplasia that would result in vein graft failure.

The present findings build upon those from Eisenhauer and colleagues [14] in several ways, including increasing the number of patients and SVGs by sixfold, expanding from single center experience to multiple centers, and evaluating of impact on clinical outcomes (both early postoperatively and longer term outcomes). Additionally, the number and location of SVGs placed during the surgery was known in the present study due to the design of the trial and the detailed surgical data collected prospectively. Therefore, all SVGs were evaluated on the follow-up angiogram. In prior SVG marker studies, it was unknown if any SVGs were missed as the extensive collection of surgical graft placement was not available. Data from the present study do not suggest a protective effect of marker use on patency, unlike the earlier study [14].

The increase in perioperative CABG MI associated with SVG radiographic marker use was unanticipated. The higher rate of perioperative CABG MI was not explained by either the longer duration of surgery or the higher frequency of urgent CABG in patients with SVG markers used, as the finding remained after adjustment in a multivariable model. While the finding may be due to chance, it is also possible that attachment of the marker may have altered local flow in the vein graft in the perioperative-maker region, and this flow disturbance may result in platelet aggregation with potential distal embolization that resulted in the increase in CKMB. Additionally, it is possible that markers could initiate a local reaction to the foreign body causing inflammation. Despite the increase in early postoperative MI with SVG markers, there was no difference in long-term mortality with SVG markers.

Limitations
Saphenous vein graft radiographic marker use was collected by the angiographic core laboratory, but specific type of marker used was not available (circumferential markers, marker clip, etc). It is possible that the type of marker used could have different effects on patency. For example, a circular ring around a vein could theoretically have a greater impact on intimal hyperplasia as compared with a metallic clip adjacent to the vein. Use of SVG markers was not randomized and was at the discretion of the surgeons. Data were not available on the duration of fluoroscopy time or the amount of contrast volume used on the follow-up angiogram, but prior studies have demonstrated that these are lower with SVG marker use. Follow-up angiograms were performed at 12 to 18 months postsurgery per the PREVENT IV protocol. It is possible that results may differ with longer angiographic follow-up. The long-term mortality analysis should be interpreted with caution because patients had to survive until the angiographic follow-up to determine if SVG markers had been placed; 91 patients in the angiographic cohort of the trial had died prior to angiographic follow-up, and status of marker use in these patients is unknown [8]. Additionally, use of SVG markers in patients who did not return for angiographic follow-up (n = 323) is unknown.

Conclusion
Saphenous vein graft radiographic marker use was not associated with an adverse effect on graft patency in a serial evaluation of more than 4,000 SVGs at 12 to 18 month postsurgery, but marker use was associated with a higher rate of ascertainment of graft patency by catheter cannulation on angiography. The SVG radiographic markers offer the benefit of increased graft visualization without an adverse effect on graft patency or long-term clinical outcomes, but the impact of the increase in perioperative CABG MI needs further examination.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Eisenhauer MD, Collier 3rd E, Eisenhauer TL, Cambier PA. Beneficial impact of aorto-coronary graft markers on post-operative angiography Cathet Cardiovasc Diagn 1997;40:249-253discussion 254.[Medline]
  2. Peterson LR, McKenzie CR, Ludbrook PA, et al. Value of saphenous vein graft markers during subsequent diagnostic cardiac catheterization Ann Thorac Surg 1999;68:2263-2266.[Abstract/Free Full Text]
  3. Gibson CM, Kirtane AJ, Murphy SA, et al. Impact of contrast agent type (ionic versus nonionic) used for coronary angiography on angiographic, electrocardiographic, and clinical outcomes following thrombolytic administration in acute myocardial infarction Catheter Cardiovasc Interv 2001;53:6-11.[Medline]
  4. Guthaner D, Wexler L. The radiologic evaluation of patients with coronary bypass Curr Probl Diagn Radiol 1976;6:1-32.[Medline]
  5. Rehani MM, Ortiz-Lopez P. Radiation effects in fluoroscopically guided cardiac interventions–keeping them under control Int J Cardiol 2006;109:147-151.[Medline]
  6. Valentin J. Avoidance of radiation injuries from medical interventional procedures Ann ICRP 2000;30:7-67.[Medline]
  7. Eisenhauer MD, Wicks AB, Olson JP, Heric B. Prevalence of aortocoronary graft marker use and the factors affecting this decision J Card Surg 1998;13:194-199discussion 200–1.[Medline]
  8. Alexander JH, Ferguson Jr. TB, Joseph DM, et al. The PRoject of Ex-vivo Vein graft ENgineering via Transfection IV (PREVENT IV) trial: study rationale, design, and baseline patient characteristics Am Heart J 2005;150:643-649.[Medline]
  9. Alexander JH, Hafley G, Harrington RA, et al. Efficacy and safety of edifoligide, an E2F transcription factor decoy, for prevention of vein graft failure following coronary artery bypass graft surgery: PREVENT IV: a randomized controlled trial JAMA 2005;294:2446-2454.[Abstract/Free Full Text]
  10. Al-Mousa EN, Dodge Jr. JT, Rizzo M, et al. Thrombolysis in myocardial infarction frame count in saphenous vein grafts Am Heart J 1998;135:323-328.[Medline]
  11. Gibson CM, Cannon CP, Daley WL, et al. TIMI frame count: a quantitative method of assessing coronary artery flow Circulation 1996;93:879-888.[Abstract/Free Full Text]
  12. Gibson CM, Cannon CP, Murphy SA, et al. Relationship of TIMI myocardial perfusion grade to mortality after administration of thrombolytic drugs Circulation 2000;101:125-130.[Abstract/Free Full Text]
  13. McCullough PA, Wolyn R, Rocher LL, Levin RN, O’Neill WW. Acute renal failure after coronary intervention: incidence, risk factors, and relationship to mortality Am J Med 1997;103:368-375.[Medline]
  14. Eisenhauer MD, Malik JA, Coyle LC, Arendt MA. Impact of aorto-coronary graft markers on subsequent graft patency: a retrospective review Cathet Cardiovasc Diagn 1997;42:259-261.[Medline]
  15. Wallitt EJ, Jevon M, Hornick PI. Therapeutics of vein graft intimal hyperplasia: 100 years on Ann Thorac Surg 2007;84:317-323.[Abstract/Free Full Text]



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T. Bruce Ferguson, Jr
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