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Ann Thorac Surg 2007;83:1024-1029
© 2007 The Society of Thoracic Surgeons


Original Articles: Cardiovascular

Gastroepiploic Artery Grafting Does Not Improve the Late Outcome in Patients With Bilateral Internal Thoracic Artery Grafting

Jiro Esaki, MDa,*, Takaaki Koshiji, MDa, Minoru Okamoto, MDa, Masaki Tsukashita, MDa, Takeshi Ikuno, MDa, Ryuzo Sakata, MDb

a Department of Cardiovascular Surgery, Kumamoto Central Hospital, Kumamoto
b Department of Thoracic and Cardiovascular Surgery, Kagoshima University Graduate School of Medical and Dental Sciences, Kagoshima, Japan

Accepted for publication October 6, 2006.

* Address correspondence to Dr Esaki, Department of Cardiovascular Surgery, Kumamoto Central Hospital, 1-5-1 Tainoshima, Kumamoto 862-0965, Japan (Email: j_esaki{at}yahoo.co.jp).


    Abstract
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Late Results
 Comment
 References
 
Background: Bilateral internal thoracic artery grafting in coronary artery bypass surgery has a better long-term outcome than single internal thoracic artery grafting. However, the efficacy of gastroepiploic artery (GEA) grafting in addition to bilateral internal thoracic artery grafting is still not well-established.

Methods: From 1989 to 1999, 311 patients underwent coronary artery bypass grafting using in situ bilateral internal thoracic arteries anastomosed to the left coronary arteries and either an in situ GEA or a saphenous vein graft (SVG) anastomosed to the right coronary artery. Ninety-nine patients using the in situ GEA (GEA group) were compared with 212 patients using the SVG (SVG group) anastomsed to the right coronary artery. Young patients and patients with hyperlipidemia were more prevalent in the GEA group.

Results: The seven-year survival rate in the GEA group and the SVG group were 94.7% and 87.2%, respectively (p = 0.068). In a multivariate analysis, the age, renal failure, and a low ejection fraction (<0.40) were all significant predictors of survival. The GEA was not a significant predictor. The seven-year freedom rates from cardiac events were similar in both groups (GEA group, 76.5%; SVG group, 78.6%; p = 0.455). The seven-year freedom rates from recurrent angina were also similar between the groups (GEA group, 85.3%; SVG group, 88.8%; p = 0.700).

Conclusions: In comparison with SVG grafting, GEA grafting to the right coronary artery did not significantly improve the late outcomes in patients with bilateral internal thoracic artery grafting.


    Introduction
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Late Results
 Comment
 References
 
Coronary artery bypass grafting (CABG) using the bilateral internal thoracic arteries (ITAs) has been demonstrated to improve survival and reduce the recurrence of angina in comparison with the CABG with a single ITA [1–5]. When bilateral ITAs are anastomosed to the left coronary arteries, several grafts can be used for the right coronary system in three-vessel disease. The right gastroepiploic artery (GEA) is an arterial graft, which can be used as an in situ graft to the right coronary artery. In addition, CABG with bilateral ITAs and GEA has been reported to have a good long-term outcome [6–9]. However, whether GEA grafting in addition to the use of in situ bilateral ITAs has a better outcome or not remains to be elucidated. We herein compared GEA grafting with saphenous vein grafting to the right coronary artery (RCA) system in the patients with bilateral ITA grafting.


    Patients and Methods
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Late Results
 Comment
 References
 
Patients
From September 1989 to December 1999, 1,426 patients underwent isolated CABG at our institution. Among them, patients with in situ bilateral ITAs anastomosed to left coronary arteries, and either an in situ GEA or a saphenous vein graft (SVG) anastomosed to the RCA system, were included in this study. Patients with both GEA and SVG anastomosed to the RCA and patients with any free arterial grafts, including free ITA grafts, were excluded. In addition, any patients who had to be operated under either ventricular fibrillation or a beating heart due to a porcelain aorta were also excluded. As a result, 99 patients with an in situ GEA (GEA group) were compared with 212 patients with a SVG anastomosed to the RCA (SVG group). Two hundred-one patients had triple-vessel disease without left main disease and 110 patients had both left main disease and RCA disease. This study was approved by the Institutional Review Board and individual patient consent was waived.

All of the operations were performed by one surgeon (R.S.). The patient characteristics are shown in Table 1. In the GEA group, the patients tended to be younger and more patients had hyperlipidemia than those in the SVG group (Table 1). The GEA, in addition to bilateral ITAs, has been used since 1994 at our institution, preferentially for younger patients. The GEA was not used if the patient had a history of a laparotomy or if the patient was presently being treated for gastric ulcers. No other preoperative comorbidity was related to the graft selection. This study includes an early experience of GEA grafting, but in the later stages of this study the GEA was not used when the degree of proximal stenosis of the target coronary artery was less than 75% because of concerns regarding the competitive flow. The size, pulsation, and calcification of the GEA were checked after laparotomy. A small or calcified or weak pulsating GEA was not harvested and instead the SVG was used for the RCA system.


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Table 1 Patient Characteristics
 
Surgical Techniques
Both the ITAs and GEA were harvested in a pedicled fashion. The ITAs were mobilized with their side branches clipped. The right GEA was then divided with the side branches ligated using 5/0 silk. The ITAs and GEA were then dilated by the intraluminal injection of papaverine.

All operations were performed under cardiopulmonary bypass with blood cardioplegia.

The left ITA was usually anastomosed to the left descending artery and the right ITA was anastomosed to the left circumflex artery through the transverse sinus (Table 2). The number of distal anastomoses was 4.0 ± 0.8 in the both groups (p = 0.984).


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Table 2 Distribution of Grafts
 
Early Study
Ninety-six percent of the patients in the GEA group and 94.8% of the patients in the SVG group underwent early postoperative angiography (p = 0.782). The mean interval of the early angiography after the operation was 12.5 ± 3.6 days. Perioperative myocardial infarction (PMI) was defined by an elevation of isoenzyme MB of creatine phosphokinase (>100) or the new Q wave in electrocardiograms.

Follow-Up
Ninety-eight percent of the patients in the GEA group and 98.6% of the patients in the SVG group were followed up based on the patients’ records and(or) a telephone interview (p = 0.655). The mean follow-up in the GEA group was 68.5 ± 24.1 months, while in the SVG group it was 88.6 ± 40.9 months (p < 0.0001).

Statistical Analysis
The patient preoperative and operative data were assessed by the t test for continuous variables, while either the {chi}2 or Fisher exact tests were used for categoric variables. In-hospital mortality was included in the survival analysis. Cardiac death included in-hospital mortality, cardiogenic death, and sudden death. Cardiac events included cardiac death (including in-hospital death) and sudden death, myocardial infarction (including in-hospital infarction), recurrent angina, repeated CABG, repeated percutaneous coronary intervention (PCI), and admission for any cardiac disease. Reintervention included repeated CABG and repeated percutaneous coronary intervention. Perioperative myocardial infarction was included in the analysis of freedom from myocardial infarction. Survival, freedom from cardiac death, freedom from cardiac events, freedom from reintervention, and freedom from myocardial infarction were all estimated by the Kaplan-Meier method and then were analyzed by the log-rank test.

Survival, freedom from cardiac events, and freedom from reintervention were analyzed by the Cox proportional hazards model. First, the patient preoperative and operative factors were analyzed by the univariate Cox proportional hazards model. Preoperative factors included age (≥70 years old), female sex, hypertension, diabetes mellitus, hyperlipidemia, history of smoking, chronic renal failure on hemodialysis, cerebrovascular disease, peripheral vascular disease, and ejection fraction (<0.40). In addition, the operative factors included GEA and grafts to the posterior descending artery or the posterolateral branch. Factors that reached significance with a probability of 0.1 were entered into the multivariate Cox proportional hazards model.

All statistical analyses were performed using the statistical software SPSS program (Dr SPSS II, SPSS Inc, Chicago, IL). A probability value less than 0.05 was considered to indicate statistical significance.


    Results
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Late Results
 Comment
 References
 
Early Result
No patients in the GEA group died, while three patients (1.4%) in the SVG group died during their hospital stay (p = 0.554). One patient died due to a cerebral infarction, one died of respiratory failure, and one died of intestinal necrosis.

Perioperative myocardial infarction occurred in six patients (6.1%) in the GEA group and in four patients (1.9%) in the SVG group (p = 0.079). No patients in the GEA group had PMI in the RCA territory, while two patients (0.9%) in the SVG group had PMI in the RCA system (p > 0.999). One patient in the SVG group required the insertion of an intraaortic balloon pump; however, no patients in the GEA group required it (p > 0.999). The other noncardiac complications included stroke in three patients (3.0%) in the GEA group and in six patients (2.8%) in the SVG group (p > 0.999), mediastinitis in two (0.9%) patients only in the SVG group (p > 0.999).

Early patencies of the left ITA to the LAD were 98.9% in the GEA group and 97.8% in the SVG group (p = 0.667). The patencies of the right ITA to the circumflex system were 98.9% in the GEA group and 97.8% in the SVG group (p > 0.999). In addition, the early patency of the GEA was 100%, while that of the SVG anastomosed to the RCA system in the SVG group was 96.6% (p = 0.111).


    Late Results
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Late Results
 Comment
 References
 
Survival
The seven-year survival rate in the GEA group was 94.7%, while that in the SVG group was 87.2% (p = 0.068) (Fig 1). In a univariate analysis, four variables (ie, GEA, age ≥70 years, renal failure, and ejection fraction <0.40) all reached significance with a probability of 0.1. These factors were thus entered into a multivariate analysis. Age, renal failure, and ejection fraction (<0.40) were found to be significant predictors of survival. However, GEA was not found to be a significant predictor (p = 0.208) (Table 3).


Figure 1
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Fig 1. Survival. (GEA = gastroepiploic artery; SVG = saphenous vein graft.)

 

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Table 3 Multivariate Analysis by Cox Proportional Hazards Model for Survival
 
Freedom From Cardiac Death
The seven-year freedom rate from cardiac death in the GEA group was 100.0%, while that in the SVG group was 95.5% (p = 0.032). An analysis by the Cox proportional hazards model was not performed due to the fact that there were no cardiac deaths in the GEA group.

Freedom From Cardiac Events
The seven-year freedom rate from cardiac events in the GEA group was 76.5%, while that in the SVG group was 78.6% (p = 0.455) (Fig 2). In a univariate analysis no variables including GEA reached a value of p less than 0.1.


Figure 2
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Fig 2. Freedom from cardiac events (including cardiac death, sudden death, myocardial infarction, recurrent angina, repeated coronary artery bypass graftin, repeated percutaneous coronary intervention and admission for any cardiac disease). (GEA = gastroepiploic artery; SVG = saphenous vein graft.)

 
Freedom From Reintervention
The seven-year freedom rate from reintervention in the GEA group was 81.9% and that in the SVG group was 85.3% (p = 0.406) (Fig 3). In a univariate analysis no variables including GEA reached a value of p less than 0.1.


Figure 3
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Fig 3. Freedom from reintervention (including repeated coronary artery bypass grafting and repeated percutaneous coronary intervention). (GEA = gastroepiploic artery; SVG = saphenous vein graft.)

 
All of the reinterventions but one were PCI. One patient with chronic renal failure in the SVG group had re-CABG concomitantly with aortic valve replacement three years after the first CABG because of severe aortic stenosis and the occlusion of the SVG to the RCA.

Freedom From Angina
The seven-year freedom rate from recurrent angina in the GEA group was 85.3% and that in the SVG group was 88.8% (p = 0.700) (Fig 4). In a univariate analysis, only peripheral vascular disease reached a value of p less than 0.1 (p = 0.055). The GEA was not a significant predictor (p = 0.700).


Figure 4
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Fig 4. Freedom from recurrent angina. (GEA = gastroepiploic artery; SVG = saphenous vein graft.)

 
Freedom From Myocardial Infarction
The seven-year freedom rate from myocardial infarction including in-hospital infarction in the GEA group was 93.9%, while that in the SVG group was 97.0% (p = 0.168) (Fig 5). An analysis by the Cox proportional hazards model was not performed due to the small number of myocardial infarctions after discharge in both groups.


Figure 5
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Fig 5. Freedom from myocardial infarction (including in-hospital myocardial infarction). (GEA = gastroepiploic artery; SVG = saphenous vein graft.)

 

    Comment
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Late Results
 Comment
 References
 
The number of percutaneous coronary angioplasties is increasing and the number of CABGs is decreasing these days because drug eluting stents are becoming more popular, and their long-term results are reported to be better than those of previous bare metal stents [10, 11]. Surgeons should therefore pursue better long-term results. The CABGs with bilateral ITAs have a better long-term outcome than CABG with a single ITA [1–5]. In addition, CABG with bilateral ITAs and GEA has been reported to have a good long-term outcome [6–9]. However, the efficacy of grafting with GEA in patients undergoing bilateral ITA grafting has not yet been clearly elucidated. Lev-Ran and colleagues [12] reported that GEA grafting to the RCA system in left-sided bilateral ITA grafting showed no particular benefit after a two-year follow-up and Pevni and colleagues [13] reported the same conclusion after a six-year follow-up, but they used many types of composite grafting. We compared GEA grafting with SVG grafting with the RCA in the patients with bilateral ITAs to the left coronary arteries for a longer follow-up. In addition, we also used no composite grafting except for one in the SVG group and our study included only CABG using in situ bilateral ITAs.

The operations were performed with a low mortality in both groups and the complications were similar between the two groups. The early patencies of ITAs, GEA, and SVGs were all satisfactory.

The survivals were not significantly different between the two groups and GEA grafting was not a significant predictor of survival in a multivariate analysis. One of the possible causes of no improvement by GEA grafting is that the long-term patency rate of GEA is not as good as that of ITA [14, 15]. Some authors [16, 17] reported the long term patency of GEA to be similar to that of SVG. Another possible cause is the small number of patients and the short-term follow-up in this study. The GEA has been used since 1994 at our hospital, so the follow-up in the GEA group was short. Because the benefit of bilateral ITA grafting over single ITA grafting has been reported to become evident from seven to 10 years after the operation [1, 4], the benefit of GEA grafting additional to bilateral ITA grafting may not become evident until more than seven to 10 years after the surgery. The rates regarding freedom from cardiac events, freedom from reintervention, freedom from recurrent angina, and freedom from myocardial infarction were similar between both groups.

The seven-year survival, seven-year freedom from cardiac events, and seven-year freedom from myocardial infarction were all comparable with other studies regarding bilateral ITAs either with or without GEA [1–4, 7, 8]. The freedom rate from reintervention in this study was less than that of other studies [1–4, 7, 8]. This is probably due to the special situation in our institution, and the situations are also the same at many other institutions in Japan. Almost all of the patients routinely undergo angiography after CABG and if any specific anastomotic stenosis is found and the target coronary artery is important, then PCI is performed even if the patient has no angina. In addition, during the follow-up if the patient has angina, angiography is often performed to check the anastomoses and to identify any new lesions. If any anastomotic failure or new lesion is found, then percutaneous coronary intervention is performed. Because reintervention was frequent, the freedom rate from cardiac events was also less than that reported in other studies.

Presently we harvest GEAs in a skeletonized fashion using ultrasound scissors. The early functionally patent rate of skeletonized GEA is reported to be better than that of nonskeletonized GEA [18]. Skeletonized GEA grafting may thus improve the late outcomes.

A limitation of this study is that it is a retrospective study and the patient characteristics were also different between the two groups due to selection bias. In addition, a small number of patients and a short follow-up time could demonstrate no difference between the two groups. A randomized large study is therefore needed before any definitive conclusions can be made.

Even though there were these limitations, the seven-year mortality and the seven-year events were compared between the groups and the seven-year follow-up is not too short to evaluate the outcome after CABG. In addition, the mean follow-up time in the SVG group was longer than five years, even though it has been reported that patency of SVG is decreased especially five years after the operation [19]. Therefore, this study has important implications regarding graft selection for the RCA system when bilateral ITAs are used.

In conclusion, GEA grafting to the RCA system, in comparison with SVG grafting, was not found to significantly improve the late outcome in CABG using bilateral ITAs.


    References
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Late Results
 Comment
 References
 

  1. Burfeind Jr WM, Glower DD, Wechsler AS, et al. Single versus multiple internal mammary artery grafting for coronary artery bypass, 15-year follow-up of a clinical practice trial Circulation 2004;110:II27-II35.[Medline]
  2. Endo M, Nishida H, Tomizawa Y, Kasanuki H. Benefit of bilateral over single internal mammary artery grafts for multiple coronary artery bypass grafting Circulation 2001;104:2164-2170.[Abstract/Free Full Text]
  3. Buxton BF, Komeda M, Fuller JA, Gordon I. Bilateral internal thoracic artery grafting may improve outcomes of coronary artery surgery, risk-adjusted survival Circulation 1998;98:II-1-II-6.[Medline]
  4. Lytle BW, Blackstone EH, Loop FD, et al. Two internal thoracic artery grafts are better than one J Thorac Cardiovasc Surg 1999;117:855-872.[Abstract/Free Full Text]
  5. Taggart DP, D’Amico R, Altman DG. Effect of arterial revascularization on survival: a systemic review of studies comparing bilateral and single internal thoracic mammary arteries Lancet 2001;358:870-875.[Medline]
  6. Nishida H, Tomizawa Y, Endo M, Koyanagi H, Kasanuki H. Coronary artery bypass with only in situ bilateral internal thoracic arteries and right gastroepiploic artery Circulation 2001;104(12 suppl 1):I76-I80.
  7. Bergsma TM, Grandjean JG, Voors AA, Boonstra PW, Heyer PD, Ebels T. Low recurrence of angina pectoris after coronary artery bypass graft surgery with bilateral internal thoracic and right gastroepiploic arteries Circulation 1998;97:2402-2405.[Abstract/Free Full Text]
  8. Tavilla G, Kappetein AP, Braun J, Gopie J, Tjien ATJ, Dion RAE. Long-term follow-up of coronary artery bypass grafting in three-vessel disease using exclusively pedicled bilateral internal thoracic and right gastroepiploic arteries Ann Thorac Surg 2004;77:794-799discussion 799.[Abstract/Free Full Text]
  9. Formica F, Ferro O, Greco P, Martino A, Gastaldi D, Paolini G. Long-term follow-up of total arterial myocardial revascularization using exclusively pedicle bilateral internal thoracic artery and right gastroepiploic artery Eur J Cardiothorac Surg 2004;26:1141-1148.[Abstract/Free Full Text]
  10. Eisenberg MJ, Konnyu KJ. Review of randomized clinical trials of drug-eluting stents for the prevention of in-stent restenosis Am J Cardiol 2006;98:375-382.[Medline]
  11. Roiron C, Sanchez P, Bouzamondo A, Lechat P, Montalesco G. Drug eluting stents: an updated meta-analysis of randomised controlled trials Heart 2006;92:641-649.[Abstract/Free Full Text]
  12. Lev-Ran O, Mohr R, Uretzky G, et al. Graft of choice to right coronary system in left-sided bilateral internal thoracic artery grafting Ann Thorac Surg 2003;75:88-92.[Abstract/Free Full Text]
  13. Pevni D, Uretzky G, Yosef P, et al. Revascularization of the right coronary artery in bilateral internal thoracic artery grafting Ann Thorac Surg 2005;79:564-569.[Abstract/Free Full Text]
  14. Suma H, Isomura T, Horii T, Sato T. Late angiographic result of using the right gastroepiploic artery as a graft J Thorac Cardiovasc Surg 2000;120:496-498.[Abstract/Free Full Text]
  15. Voutilainen S, Verkkala K, Jarvinen A, Keto P. Angiographic 5-year follow-up study of right gastroepiploic artery grafts Ann Thorac Surg 1996;62:501-505.[Abstract/Free Full Text]
  16. Hirose H, Amano A, Takanashi S, Takahashi A. Coronary artery bypass grafting using the gastroepiploic artery in 1,000 patients Ann Thorac Surg 2002;73:1371-1379.[Abstract/Free Full Text]
  17. Hirose H, Amano A, Takahashi A. Bypass to the distal right coronary artery using in situ gastroepiploic artery J Card Surg 2004;19:499-504.[Medline]
  18. Kamiya H, Watanabe G, Takemura H, Tomita S, Nagamine H, Kanamori T. Skeletonization of gastroepiploic artery graft in off-pump coronary artery bypass grafting: early clinical and angiographic assessment Ann Thorac Surg 2004;77:2046-2050.[Abstract/Free Full Text]
  19. Fitzgibbon GM, Kafka H, Leach AJ, Keon WJ, Hooper D. Coronary bypass graft fate and patient outcome: angiographic follow-up of 5065 grafts related to survival and reoperation in 1388 patients during 25 years J Am Coll Cardiol 1996;28:616-626.[Abstract]

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