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Ann Thorac Surg 2006;81:2135-2141
© 2006 The Society of Thoracic Surgeons

Original article: Cardiovascular

Right Gastroepiploic Artery for Revascularization of the Right Coronary Territory in Off-Pump Total Arterial Revascularization: Strategies to Improve Patency

Ki-Bong Kim, MD, PhD * , Kwang Ree Cho, MD, Jae-Sung Choi, MD, Hyun-Joo Lee, MD

Department of Thoracic and Cardiovascular Surgery, Seoul National University Hospital, Seoul, Korea

Accepted for publication January 9, 2006.

* Address correspondence to Dr Kim, Department of Thoracic and Cardiovascular Surgery, Seoul National University Hospital, 28 Yeun-Kun Dong, Chong-Ro Ku, Seoul 110-744, Korea. (Email: kimkb{at}snu.ac.kr).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: We evaluated the early and 1-year postoperative results of grafting the skeletonized right gastroepiploic artery to the right coronary territories.

METHODS: One hundred and seventy-five patients who underwent off-pump total arterial revascularization using the skeletonized right gastroepiploic artery and bilateral internal thoracic arteries were studied. The right gastroepiploic artery was used for revascularizing the right coronary territories, and bilateral internal thoracic arteries were used for revascularizing the left coronary territories. We revised the in-situ right gastroepiploic artery graft into a composite or free graft if the flowmeter measurement suggested a competitive flow pattern. Postoperative angiographies were performed in 98.3% of the patients before discharge, and in 92.0% of the patients 1 year after surgery.

RESULTS: Hospital mortality was 0.6%. Postoperative angiography showed early patency rate of 98.3% for the right gastroepiploic artery and 99.4% for the internal thoracic artery (p = 0.352), and 1-year patency rate of 92.0% for the right gastroepiploic artery and 97.2% for the internal thoracic artery (p = 0.009). Flow competition of the right gastroepiploic artery was observed in 5.2% of the patients at the early postoperative angiography and in 6.8% of the patients 1 year after surgery. The incidence of right gastroepiploic artery graft flow competition was significantly decreased compared with that of the pre–flowmeter period (p = 0.036 at early angiography; p = 0.017 at 1-year angiography).

CONCLUSIONS: The skeletonized right gastroepiploic artery grafted to the right coronary territory demonstrated excellent early and 1-year patency rates. Flow competition of the in situ right gastroepiploic artery may be overcome by intraoperative revision of graft based on flow measurement.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Enhanced long-term survival and greater freedom from reinterventions have been shown when bilateral internal thoracic arteries are used rather than a single internal thoracic artery (ITA) in patients with triple-vessel disease [1]. In addition, the surgical results of off-pump coronary artery bypass graft surgery (OPCABG) have demonstrated several advantages by avoiding the potentially detrimental effects of cardiopulmonary bypass and eliminating intraoperative global myocardial ischemia [2, 3]. These recent advances in the field of coronary artery surgery have increased surgeon interest in OPCABG using purely arterial grafts because of its low morbidly and improved long-term myocardial revascularization outcome. However, the complementary graft of choice to the right coronary artery territory in patients undergoing left-sided bilateral ITA grafting remains controversial [4].

The aims of this study were (1) to evaluate the early and midterm results of total arterial OPCABG using the skeletonized right gastroepiploic artery (RGEA) for revascularization of the right coronary territory, and (2) to demonstrate if the flow competition of the RGEA graft may be overcome by intraoperative flow measurement and graft revision.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Patient Characteristics
A total of 175 consecutive patients who underwent OPCABG for multivessel coronary artery disease using a skeletonized RGEA and bilateral ITAs between August 1999 and December 2003 were studied (Table 1). A computer-based patient database system was used for this study. The study protocol was reviewed by the Institutional Review Board and approved as a minimal risk retrospective study (Approval Number: H-0512-504-163) that did not require individual consent based on the institutional guidelines for waiving consent.


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  		Table 1. Preoperative Characteristics and Risk Factors of the Study Patients
 
A skeletonized RGEA was used for revascularization of the right coronary territory and bilateral ITAs were used for revascularization of the left coronary territory. These 175 OPCABGs were 29.6% (175 of 591) of the total isolated OPCABGs performed during the same period. Two hundred and thirty of 591 patients (38.9%) had multivessel disease requiring revascularization of all the three-vessel territories. Patients who underwent OPCABG using a saphenous vein graft, or OPCABG using a single ITA and RGEA were excluded from the study. All patients stopped taking aspirin the day before surgery and resumed aspirin (300 mg/d) beginning 1 day postoperatively.

Early postoperative angiographies (postoperative 1.3 ± 0.9 days) were performed in 98.3% (172 of 175) of the patients, and postoperative 1-year angiographies (12.9 ± 6.2 months postoperatively) were performed in 92.0% (161 of 175) of the patients, regardless of the patient's anginal symptoms. Patients who died, refused angiographic evaluation, or had renal function impairment were excluded from the angiographic follow-up data. Follow-up coronary angiography included four-plane selective coronary and bypass graft angiography. One physician initially reviewed all the coronary angiograms and consensus was reached after review. Graft patency was graded as described by FitzGibbon and associates (grade A = excellent; grade B = fair; grade A+B = patent) [5]. Competitive graft flow was defined as distal native grafted coronary artery flow not clearly opacified as seen by graft angiography, but well-visualized graft retrogradely as seen by native coronary angiography. If the distal graft as well as the native coronary artery was not opacified as seen by graft angiography, it was classified as a grade B anastomosis.

The operations were all performed by a single surgeon (K.-B. K.).

Surgical Technique
The OPCABG was performed as previously described [6]. The patients were given heparin with an initial dose of 1.5 mg/kg of heparin and periodically received supplemental doses to maintain an activated clotting time of more than 300 seconds. Bilateral ITAs were initially harvested using a standard skeletonizing technique in all patients. If using bilateral ITAs as in situ or Y grafts did not achieve complete revascularization, a short lower extension (3 to 5 cm) of the median incision was made to harvest the RGEA in a skeletonized fashion. After opening the peritoneal cavity, the RGEA was exposed by incising the anterior layer of the greater omentum by electrocautery. Scissors or the tip of the cold cautery device were used to free the RGEA from the accompanying vein and to identify the side branches to the stomach and omentum. All branches were occluded with the use of two surgical clips on each side to the stomach and omentum, and were divided by scissors. The RGEA was approached from the posterior aspect of greater omentum, and dissected proximally to the pylorus and then leftward two thirds of the distance along the great curvature of the stomach. Throughout the dissection, the grafts were sprayed with warm diluted papaverine solution to minimize spasm and to prevent desiccation. After systemic heparinization, the grafts were clipped distally. The grafts were then immersed in a 10-mL syringe filled with warm diluted papaverine saline solution (1 mg/mL) and allowed to pharmacologically dilate until use. Intraluminal injection of papaverine solution was not used. The in-situ RGEA was routed anterior to the pylorus, and the left lobe of the liver to the pericardial cavity. An incisional opening in the diaphragm was made using the electrocautery to reach the target vessel without torsion or tension based on the site of the target coronary artery. Protamine was not given at the end of the procedure.

Revascularization Strategies
Bilateral ITAs were preferred for use as in-situ grafts for revascularization of the left coronary territory. The right ITA was used to revascularize the left anterior descending artery by crossing the midline, the ramus, or high obtuse marginal branch through the transverse sinus as an in-situ graft. If the right ITA was too short to reach the left coronary territory or if the left coronary territory could not be completely revascularized with bilateral in-situ ITA grafts, a Y-composite graft was constructed before starting the distal anastomoses. Bilateral ITAs were used as in-situ grafts in 35.4% (62 of 175) of the patients and as Y-composite graft in 64.6% (113 of 175) of the patients.

If use of the bilateral ITAs as in-situ or Y grafts did not achieve complete revascularization, the RGEA was used for revascularization of the right coronary territory that had more than 80% stenosis. The RGEA was preferred for use as an in-situ graft for revascularization of right coronary territory under the assumption that multiple blood sources were better than one.

If significant narrowing of the celiac axis was found on the preoperative abdominal aortogram or thoracoabdominal computed tomography, or if intraoperative flow measurement suggested a competitive flow pattern, the RGEA was used as a composite graft or free graft instead of an in-situ graft. The RGEA with a diameter greater than 2.0 mm or devoid of palpable atheroma was used as a graft. When we evaluated the suitability of RGEA grafts in 59 consecutive patients (male:female = 42:17) during the study period, 10 patients (16.9%) demonstrated unsuitable RGEA grafts (6 for multiple atherosclerotic plaques; 4 for small-caliber artery). Since the introduction of transit time flow measurement (TTFM [BF1001; Medi-Stim AS, Oslo, Norway]) at our institute in October 2000, we derived the following criteria to predict abnormal grafts (occluded or competitive grafts) from four variables that could be displayed simultaneously on a real-time screen [7]: (1) systolic dominant or balanced pattern of the flow curve in the left coronary territories, systolic dominant pattern of the flow curve in the right coronary territories; (2) mean flow less than 15 mL/min; (3) pulsatility index greater than 3 in the left coronary territories and greater than 5 in the right coronary territories; and (4) insufficiency ratio greater than 2%.

The differentiation between the competitive and occluded grafts was performed by proximal snaring of the native coronary artery in conjunction with the analysis of the TTFM variables, or by calculating the fast Fourier transformation ratio of less than 1 to differentiate the occluded from normal grafts. If there was suspicious flow competition, the in-situ RGEA was divided at its proximal section and anastomosed to the side of the left ITA in a Y-composite fashion or to the side of the ascending aorta after construction of a pericardial aortic patch (Fig 1). The RGEA was used as an in-situ graft in 85.7% (150 of 175) of the patients, a composite graft in 9.1% (16 of 175) of the patients, and a free graft in 5.1% (9 of 175) of the patients. The reasons for using the RGEA as a composite or free graft were suspicious competition on intraoperative TTFM (n = 14), short or diseased RGEA (n = 5), celiac axis narrowing found in preoperative evaluation (n = 4), and prearranged abdominal surgery (n = 2).


Figure 1
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  		Fig 1. Intraoperative transit time flow measurement findings. (A) Competitive flow was suggested when the right gastroepiploic artery was grafted to the posterior descending artery as an in-situ graft. Before revision, pulsatility index (PI) value = 6.7, mean flow = 8 mL/min. (B) The right gastroepiploic artery was divided at its proximal section and anastomosed onto the ascending aorta as a free graft, and the flowmeter demonstrated an improved flow pattern. After revision, pulsatility index value = 1.5, mean flow = 20 mL/min.

 
Statistical Analysis
Statistical analysis was performed with the SPSS software package (version 11.0; SPSS, Chicago, IL). Comparison of patency rates and flow competition was performed using the {chi}2 test (Pearson chi and Fisher's exact tests), and serial angiographic comparisons of the graft patency and prevalence of competitive flow in patients who had both the early and 1-year coronary angiographies (n = 160) were performed using the {chi}2 test (McNemar test). Comparison of the free graft flow was performed using one-way analysis of variance (ANOVA) with post hoc multiple comparison (Tukey). All results were expressed as mean ± SD, and a p value of less than 0.05 was considered to be statistically significant.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Free Flow of Arterial Grafts and Distal Anastomoses
In 2003, we measured the free flow of grafts just before performing distal anastomosis in 30 patients who received bilateral ITAs as a Y-composite graft and the RGEA as an in-situ graft, respectively. The RGEA grafts showed a higher free flow (107 ± 66 mL/min) than the left ITA grafts (91 ± 47 mL/min; p = 0.517) and a lower free flow than the Y-composite grafts (120 ± 51 mL/min; p = 0.660) with no statistical significance, while mean blood pressure was maintained between 80 and 90 mm Hg (Table 2). The average number of distal anastomoses per patient was 3.7 ± 0.7. The average number of distal anastomoses per bilateral ITA was 2.7 ± 0.7, and the average number of distal anastomoses using the RGEA was 1.0 ± 0.1. All the RGEA were anastomosed to the right coronary artery territory; right coronary artery in 17 patients, posterior descending artery in 151 patients, and posterolateral branch in 8 patients (Table 3). Both the posterior descending artery and posterolateral branch were grafted with an in-situ RGEA in 1 patient.


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  		Table 2. Operative Data
 

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  		Table 3. Target Coronary Territories by Internal Thoracic Artery (ITA) and Right Gastroepiploic Artery (RGEA)
 
Mortalities and Morbidities
Operative mortality rate was 0.6% (1 of 175). There were four additional late deaths during the first postoperative year; the causes of death were pneumonia (n = 1), accident (n = 1), lung cancer (n = 1), and abdominal aortic aneurysm rupture (n = 1). Postoperative morbidities were atrial fibrillation (n = 31, 17.7%), bleeding requiring reoperation (n = 7, 4.0%), transient acute renal failure (n = 4, 2.3%), perioperative myocardial infarction (n = 3, 1.7%), mediastinitis (n = 1, 0.6%), acute gastric mucosal lesion (n = 1, 0.6%), and splenic capsular tearing (n = 1, 0.6%). There was no postoperative low cardiac output syndrome or stroke (Table 4).


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  		Table 4. Postoperative Data: Mortalities, Morbidities, and Hospital Course
 
Immediate Postoperative and 1-Year Angiographies
Early postoperative angiographies demonstrated a 99.4% (464 of 467) patency rate for ITA grafts and 98.3% (170 of 173) patency rate for RGEA grafts (p = 0.352; Table 5). Postoperative 1-year angiographies demonstrated a 97.2% (424 of 436) patency rate for ITA grafts and 92.0% (149 of 162) patency rate for RGEA grafts (p = 0.009). All the occluded RGEA grafts (3 in early angiography; 13 in 1-year angiography), except 1 Y-composite graft in the 1-year angiography, were in-situ grafts. Nine of 173 (5.2%) RGEA grafts in the early postoperative angiography and 11 of 162 (6.8%) RGEA grafts in the 1-year angiography showed a competitive flow pattern. Of nine competitive RGEA grafts examined by early postoperative angiography, there were 6 RGEA grafts (5 in-situ RGEAs and 1 Y-composite RGEA) anastomosed to the posterior descending artery (6 of 151), and 3 in-situ RGEA grafts anastomosed to the right coronary artery (3 of 17). The RGEA graft anastomosed to the right coronary artery showed a higher incidence of competitive graft flow than grafts anastomosed to the posterior descending artery (3 of 17 versus 6 of 151; p = 0.050). When the free flow of RGEA graft measured just before performing distal anastomosis was compared with patients who had competitive RGEA grafts and those with FitzGibbon grade A grafts, the former showed a lower free flow than the latter (86 ± 59 mL/min versus 140 ± 91 mL/min; p =0.059).


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  		Table 5. Postoperative Angiographic Patency Rates: Results Early and One Year After Surgery
 
We compared the incidence of flow competition before and after the introduction of TTFM at our institute in October 2000, the point at which the in-situ RGEA began being revised in cases of suspicious flow competition. Early postoperative angiographies demonstrated that 14.8% (4 of 27) and 3.5% (5 of 144) of the RGEA grafts showed competitive flow patterns before and after the introduction of TTFM, respectively (p = 0.036). Postoperative 1-year angiographies demonstrated 19.2% (5 of 26) and 4.4%(6 of 136) of the RGEA grafts showed competitive flow patterns before and after the introduction of TTFM, respectively (p = 0.017). Early and 1-year postoperative angiographies demonstrated that intraoperative revision of in-situ RGEA grafts significantly decreased the incidence of competitive flow patterns.

Of the 175 patients, 160 patients who received both postoperative early and 1-year coronary angiographies were analyzed for serial comparison (Table 6). Although the patency rates of ITA (99.3%, 431 of 434 versus 97.2%, 422 of 434; p = 0.012) and RGEA grafts (98.8%, 159 of 161 versus 91.9%, 148 of 161; p = 0.001) were significantly decreased from early postoperatively to 1 year after surgery, the prevalence of competitive flow in the RGEA graft remained stable (5.6%, 9 of 161 versus 6.8%, 11 of 161; p = 0.774; Table 6).


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  		Table 6. Postoperative Patency Rates: Serial Angiographic Comparison
 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
This study revealed two main findings. First, the skeletonized RGEA was a suitable arterial graft for revascularization of the right coronary territory in terms of low surgical risk, high patency rate, and excellent patient outcome. Second, intraoperative revision based on intraoperative flow measurement may decrease the incidence of flow competition in the in-situ RGEA graft.

The skeletonized technique for harvesting bilateral ITAs has allowed the dissected ITA to be longer and have greater spontaneous blood flow, making bilateral ITAs useful as grafts to all necessary vessels requiring surgical revascularization [6, 8, 9]. However, even the use of skeletonized bilateral ITAs is not always enough to accomplish total arterial revascularization in multi-vessel coronary artery disease. When bilateral ITAs are used for left-sided revascularization, other arterial conduits that may be used to revascularize the right coronary artery territory are the RGEA, radial artery, and free right ITA. Although total arterial revascularization of the total coronary system has demonstrated good clinical results and excellent revascularization patency rates [10–12], the patency rate of conduits grafted to the right coronary artery territory had any disappointing results [13, 14], and some reports even failed to demonstrate benefits of arterial grafts over saphenous vein grafts [4, 15, 16].

The RGEA has several advantages as an arterial graft, such as an arterial conduit that enables comparable size artery-to-artery anastomosis, no additional incision needed in the leg or forearm, possible simultaneous harvesting along with ITA, avoidance of aortic manipulation, and another source of blood supply as an in-situ graft [17]. Although the RGEA has been used as a suitable conduit for coronary artery bypass surgery in terms of low surgical risk, high patency rate, and excellent patient outcome [10, 11, 18], the possibilities of coronary flow competition [19, 20] and insufficient flow capacity [21] have been indicated as limitations of the RGEA graft. The development of flow competition has been suggested as a cause of graft failure, with a temporal relationship between competitive flow and prognosis of the conduit [20]. Experience with ITA skeletonization prompted surgeons to harvest the RGEA in a similar manner in order to gain the advantages of skeletonization. By using a skeletonized RGEA, there are further advantages, such as avoidance of early spasm, easy identification of potential bleeders, quality of the vessel, functionally lengthened and larger graft, ease in performing sequential anastomosis, and preservation of lymphatic and venous drainage to the stomach [22, 23]. In the present study, skeletonization offered a large RGEA with a luminal diameter of greater than 2 mm at the distal end of the anastomosis in most of the patients. By using the skeletonized RGEA for revascularization of the right coronary artery territory, the present study demonstrated an RGEA early postoperative patency rate comparable to that of the ITA (98.3% versus 99.4%, p = 0.352), although it became lower than that of the ITA at 5 years postoperatively (92.0% versus 97.2%, p = 0.009).

Even though the RGEA has a high free flow, it may have a limited ability to supply blood to the diastolic-dominant coronary circulation as an in-situ graft because the RGEA is the fourth branch originating from a systolic-dominant circulation far away from the heart [24]. To avoid a setting with possible flow competition, it has been recommended that the RGEA not be used as an in-situ graft if the inner diameter at the anastomotic site is less than 1.5 mm and the free flow is less than 120 mL/min [25]. The present study also showed that the RGEA graft with a lower free flow showed a higher tendency of flow competition; in addition, the RGEA graft anastomosed to the right coronary artery rather than the posterior descending artery showed a higher incidence of flow competition. These findings supported the hypothesis that the RGEA might have a limited ability to supply blood to the diastolic dominant proximal coronary circulation as an in-situ graft.

In addition, the prevalence of significant celiac axis stenosis was reported as 7.3% (29 of 400 patients) in a Korean population, although it was lower than the previously reported incidence of celiac axis stenosis in Western populations (12.5% to 24%) [26]. If significant narrowing of the celiac axis was found on the preoperative abdominal aortogram or thoracoabdominal computed tomography, we used the RGEA as a composite or free graft to avoid possible flow competition that would result in graft failure.

Since the introduction of TTFM at our institute, we derived criteria to predict abnormal grafts [7]. The differentiation between the competitive and occluded grafts was performed by proximal snaring of the native coronary artery in conjunction with the analysis of the flowmeter variables, or by calculating the fast Fourier transformation ratio of less than 1 to differentiate occluded from normal grafts. Fourteen in-situ RGEA grafts were revised into composite or free grafts based on the flowmeter measurement in the present study. When we compared the incidence of flow competition of the in-situ RGEA graft before and after the introduction of flowmeter, development of flow competition decreased significantly after 1 year (19.2% versus 4.4%, p =0.017) as well as at the early (14.8% versus 3.5%, p = 0.036) postoperative angiographies.

In conclusion, the skeletonized RGEA demonstrated excellent early and 1-year patency rates and could be used for arterial revascularization of the right coronary territory. Flow competition of the in-situ RGEA may be overcome by intraoperative revision of graft based on the flow measurement.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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Ki-Bong Kim
Kwang Ree Cho
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ANN THORAC SURG ASIAN CARDIOVASC THORAC ANN EUR J CARDIOTHORAC SURG
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