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Ann Thorac Surg 2002;73:1371-1379
© 2002 The Society of Thoracic Surgeons
a Department of Cardiovascular Surgery, Kobari General Hospital, Chiba, Japan
b Department of Cardiovascular Surgery, Shin-Tokyo Hospital, Chiba, Japan
Accepted for publication January 4, 2002.
* Address reprint requests to Dr Hirose, Department of Cardiovascular Surgery, Kobari General Hospital, 29-1 Yokouchi, Noda City, Chiba 278-8501, Japan
e-mail: genex{at}nifty.com
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Abstract |
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Methods. Between June 1, 1991, and June 30, 2001, 1,000 consecutive isolated coronary artery bypass grafting procedures using the GEA were performed in the Shin-Tokyo Hospital Group. The perioperative data were retrospectively analyzed, and the late angiographic results, cardiac related events, and survival were examined. The end points of the follow-up study were death or the occurrence of a cardiac-related event.
Results. The GEA was used in 767 men and 233 women (mean age, 63.8 ± 9.4 years). The GEA was used as an in situ graft in 99.6% of patients and was anastomosed to the right coronary artery in 87.8% and the circumflex artery in 10.0%. In addition, the left internal mammary artery was used in 96.9% of patients, the right internal mammary artery in 28.5%, the radial artery in 41.7%, the inferior epigastric artery in 1.4%, and the saphenous vein in 40.1%. The hospital morbidity and mortality rates were 10.8% and 0.8%, respectively. No abdominal complications were observed. Postoperative myocardial infarction associated with GEA graft failure occurred in 2 patients. During the late follow-up of 4.0 ± 2.3 years, cardiac-related events were observed in 155 patients. The actuarial 3- and 5-year event-free rates were 91.2% and 84.2%, respectively. There were 86 late deaths, 36 of which were cardiac related deaths. The actuarial 3- and 5-year survival rates were 96.6% and 92.6%, respectively. Angiography was performed on 437 patients within 1 year after operation and in 221 patients more than 1 year postoperatively (mean interval, 3.1 ± 1.8 years). The actuarial 1-, 3-, and 5-year GEA graft patency rates were 98.7%, 91.1%, and 84.4%, respectively, and the actuarial 1-, 3-, and 5-year LIMA graft patency rates were 99.6%, 98.8%, and 97.0%, respectively (p < 0.0005).
Conclusions. The GEA was used for coronary artery bypass grafting with good perioperative results. However, the angiographic patency rate of the GEA was inferior to that of the internal mammary arteries. The late occurrence of angina attributed to GEA graft failure should be carefully monitored.
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Introduction |
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(LIMA) rather than a saphenous vein graft on the left anterior descending coronary artery (LAD) has been clearly demonstrated [4]. The second choice of arterial graft after the LIMA is controversial. In our institution, the gastroepiploic artery (GEA) has commonly been used. Over 10 years, 1,000 patients underwent isolated CABG with the GEA. A retrospective study was performed to determine the postoperative outcomes of these patients after GEA grafting.
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Material and methods |
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Preoperative exclusion criteria for GEA harvesting were as follows: previous upper abdominal operation (excluding laparoscopic procedure); previous gastrectomy, active peptic ulcer, and presence of an upper abdominal mass. The techniques of CABG with the GEA have been described elsewhere [5, 6]. Briefly, the abdominal cavity was entered by extending the median sternotomy a few centimeters caudally. The stomach was pulled up anteriorly, and the GEA was evaluated by finger palpation. Intraabdominal adhesion and the presence of a mass were sought. If there was extensive adhesion around the stomach or a palpable mass in the stomach or liver, GEA harvest was abandoned, and alternative conduits were taken.
Dissection of the GEA was carried out proximally to the pylorus ring and distally to the midportion of the greater curvature of the stomach. All gastric branches were ligated with hemoclips or, more recently with an ultrasonic scalpel. After heparin sodium was administered, the GEA pedicle was transected. Diluted papaverine hydrochloride (1:10) was injected into the pedicle through the distal stump, and the stump was then clipped until use. The harvested pedicle was wrapped in a warm papaverine-soaked sponge. Passed in front of the stomach and liver, the GEA pedicle was pulled up to the pericardial cavity through a small hole made in the middle of the diaphragm. In most cases, the GEA was used as an in situ bypass graft. Coronary artery bypass grafting was performed with cardioplegic arrest at normothermia (36°C) and cardiopulmonary bypass. After September 1996, off-pump CABG was adopted and selected patients were referred to off-pump CABG on a beating heart [7].
The bypass target of the GEA was mainly the right coronary artery (RCA) because of the limitation of graft length. If a long GEA was available, the target was extended to the circumflex system. In situ grafting was favored for patients with a calcified aorta. In the case of a high-flow coronary artery with mild stenosis, the saphenous vein was used instead of the GEA.
Early angiography (within 1 year after operation) was performed if the patient agreed to the procedure. Late coronary angiography (2 to 3 years postoperatively) was proposed for all patients followed up at our institution. Follow-up angiography was strongly recommended for all patients with symptoms of angina. Because only 10% of the patients were followed up at our institution, the timing of late angiography varied depending on the follow-up private physicians. The quality of the anastomosis was graded according to the classification of Fitzgibbon and colleagues [8]. Diffuse graft narrowing (string sign) or anastomosis stenosis was classified as grade B anastomosis.
By retrospective chart review, the following variables were collected: age, sex, results of preoperative angiography, cardiac profile, preoperative risk factors, graft material, surgical data, postoperative complications, and mortality. Major complications were defined as life-threatening complications: low-output syndrome, myocardial infarction (new Q wave), respiratory failure (ventilator support 
5 days or reintubation), pneumonia, cerebral vascular accident, reoperation for bleeding, postoperative renal failure required hemodialysis, mediastinitis, and severe arrhythmia (ventricular tachycardia, arrest, complete atrioventriicular block, or need of pacemaker implantation). Follow-up information was collected by direct patient contact, by mailed questionnaires, or by contact with the private cardiologists. Cardiac-related events after hospital discharge, were noted and included myocardial infarction, angina, arrhythmia requiring hospitalization, congestive heart failure requiring hospitalization, native coronary artery or graft stenosis requiring any type of coronary intervention, and sudden death. These follow-up data were compiled by August 31, 2001. The end points were death or occurrence of a cardiac-related event.
Results are expressed as the mean ± the standard deviation. Postoperative patient survival, event-free rate, and long-term graft patency were calculated using the Kaplan-Meier method. All statistical analyses were performed using Statview version 5.0 (SAS Institute, Cary, NC).
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Hospital results
Postoperative data are listed in Table 4.
There were 8 hospital deaths (hospitality mortality rate, 0.8%). There were 108 patients with major complications (morbidity rate, 10.8%). No abdominal complications, such as bowel obstruction, incisional hernia, delay of feeding, or gastroduodenal bleeding, were observed. Gastroepiploic artery-related postoperative myocardial infarction occurred in 2 patients. One infarction was due to graft occlusion, and the patient underwent redo CABG using a saphenous vein graft on postoperative day 3. The other was caused by GEA spasm, confirmed by angiography on postoperative day 5. The patient was treated with an intraaortic balloon pump and aggressive use of an antispasmodic agent. Repeat angiography at 6 months demonstrated complete resolution of the GEA spasm, and the graft appeared to be patent.
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Late results
Postoperative follow-up was complete for all hospital survivors (mean follow-up, 4.0 ± 2.3 years). During follow-up, cardiac-related events occurred in 155 patients (15.6%), including recurrence of angina in 57, acute myocardial infarction in 4, congestive heart failure in 39, need of percutaneous transluminal coronary angioplasty in 49, arrhythmia requiring hospitalization in 17, and sudden death in 13 (Table 5).
Percutaneous transluminal coronary angioplasty was performed for a new lesion in the coronary artery in 26 patients and graft stenosis or occlusion-related ischemia in 23. The frequency of percutaneous transluminal coronary angioplasty related to the LIMA, the RIMA, the radial artery, the GEA, and the saphenous vein was 44.1% (437/992) (three instances of angioplasty because of LIMA failure among 961 follow-up patients who had had LIMA grafting), 0.35% (1/284), 0.24% (1/414), 1.1% (11/992), and 1.8% (7/398), respectively. Actuarial 1-, 3-, 5-, and 7-year event-free rates were 97.2%, 91.2%, 84.2%, and 77.0%, respectively (Fig 1).
During the same follow-up period, there were 86 deaths (8.7%), including 36 cardiac-related deaths. Actuarial 1-, 3-, 5-, and 7-year survival rates after CABG were 99.2%, 96.6%, 92.6%, and 87.7%, respectively (Fig 2).
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1 year after CABG) at a mean interval of 3.1 ± 1.8 years. Among these patients, 77 had repeat angiography. Late angiography revealed an additional 20 GEA anastomotic occlusions and 32 grade B anastomoses, for an anastomosis patency rate (grades A + B) of 91.8%, and a stenosis-free patency rate (grade A) of 78.6% (see Table 6). Twenty patients showed late occlusions of GEA grafts, seven patients had good native coronary flow with less native coronary artery stenosis compared with preoperative angiographic studies. Four late graft occlusions were related to progression of the anastomotic stenosis, which was identified in early angiography. The other nine late graft occlusions occurred without clear reasons; five grafts were widely patent at early angiography and found to be occluded at late angiography, and four grafts were found to be occluded at the initial angiographic evaluation more than 1 year after operation. At late angiography, 17 anastomotic stenoses were observed, including eight noted in previous angiographic examinations. Late string signs were found in 15 GEA grafts; high native coronary flow was observed in 9 patients, competitive bypass flow was seen in 1 patient, and the reasons could not be determined in 5. Among the 71 patients who received sequential GEA grafts, 47 underwent postoperative angiography, and only one graft was found to be occluded 1 year after CABG. The patient had undergone GEA-circumflex-circumflex bypass grafting. The most distal limb of the graft was occluded, but the proximal GEA-circumflex bypass graft was patent.
The actuarial graft patency rates were calculated with the Kaplan-Meier method, which revealed that the 1-, 3-, and 5- year patency rates of the GEA were 98.7%, 91.1%, and 84.1%, respectively. Graft patency of the GEA and other conduits is shown in Table 6 and Figure 3. The 3-year graft patency rates of the LIMA, the RIMA, the radial artery, the GEA, and the saphenous vein were 98.8%, 98.2%, 91.3%, 91.1%, and 90.6%, respectively (p < 0.001). The GEA graft patency rate was significantly inferior to that of the LIMA or the RIMA (p < 0.0005), but it was not significantly different from that of the radial artery or the saphenous vein graft.
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Comment |
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Harvest of the GEA requires a laparotomy, which can be performed by extension of the midsternal incision. The reported abdominal complications include gastric perforation [11], bleeding from a gastric ulcer [12], incisional hernia [13], and pancreatitis [5], but none of them occurred in our series. The time required for GEA harvesting is about 20 minutes, which is almost the same as for IMA harvest. Previous abdominal operation is not a contraindication to GEA harvesting. However, intraabdominal adhesion can result in a prolonged time for GEA harvest and can cause accidental graft injury. Another contraindication to GEA harvesting is the presence of an upper abdominal malignancy. Because lymphatic metastasis can occur by way of the GEA, the GEA may be sacrificed for lymph node dissection. We [14] twice have incidentally found gastric cancer during GEA harvest. In neither patient was the GEA used for CABG, and an alternative graft was chosen. We also have had 2 patients in whom gastric tumor was found a few years after GEA grafting. One of them had early gastric cancer treated with a simple gastrectomy with minimal lymph node dissection and preservation of the GEA. The other was treated with percutaneous transluminal coronary angioplasty of the native coronary artery prior to the gastric surgical procedure, and gastrectomy was performed with ligation of the GEA.
Histologically the GEA is classified as a muscular artery [15], which places it in a similar category as the radial artery and the inferior epigastric artery. One of the clinical characteristics of a muscular artery is vasospasm: constriction of the smooth muscles in the media resulting in the narrowing of the luminal diameter and the subsequent decrease of blood flow delivery. Vasospasm can be provoked by mechanical stimuli, such as electrocautery or direct handling of the arterial wall. Unexpected bleeding from the gastric branches because of inadequate hemostasis can also induce spasm. To avoid intraoperative vasospasm, hemostasis should be accomplished with metal clips or ultrasonic scalpels, and use of the electrocautery should be minimized. Because the distal lumen is more prone to spasm, some degree of spasm occur after GEA harvest. An intraluminal injection of papaverine plays an essential role in reversing the vasospasm.
A GEA with a small diameter should not be used as a graft. Ochi and co-workers [16] reported that a GEA with a luminal size smaller than 2 mm is unable to provide enough graft flow to improve the motion of the ischemic myocardium. Nishida and associates [17] recommended a GEA diameter of 2.0 mm or more to avoid early graft closure. In Japanese patients, the GEA is usually at least 1.5 mm [18]. We use GEAs with an external diameter greater than 1.5 mm at the time of the first examination, rather than after harvest. In our experience, GEAs with a 1.5-mm diameter can be dilated to 2.0 to 2.5 mm after an intraluminal injection of papaverine. If the GEA appears smaller than 1.5 mm or weak in pulsation at the time of examination, it should not be used, and an alternative conduit should be harvested. As the luminal diameter and the length of the GEA are not as consistent as those of the IMA, some researchers [16] recommend preoperative GEA angiography. However, selective angiography of the GEA is technically difficult, whereas intraoperative examination of the GEA is easy and is sufficient to evaluate the quality of the graft. Thus, we do not routinely require preoperative angiography.
We use the in situ GEA mostly for revascularization of the distal RCA, usually the posterior descending artery. Although Suma and colleagues [6] reported that the GEA can be used as a graft on the LAD, we have found no clinical benefit of GEA-LAD bypass grafting except in special circumstances, such as a redo CABG where the IMA has been used previously and where the ascending aorta is severely calcified, or single RCA revascularization with the off-pump technique through a subxiphoid approach. In our protocol, the LAD is revascularized with one of the IMAs. The GEA can serve as a bypass graft on the circumflex artery, but that artery is often beyond the reach of an in situ GEA. We do not skeletonize the GEA because of the risk of vasospasm. Thus, bypass grafting on the circumflex artery is usually accomplished with the radial artery or saphenous vein. The patency rate of the free GEA is reported to be insufficient for an in situ graft [19] and therefore almost all GEAs are used as in situ grafts. The length of an in situ GEA is always adequate for bypass, grafting on the RCA; we have never seen a GEA too short to reach the RCA. Revascularization of the RCA system can be carried out using a wide selection of grafts: the GEA, the RIMA, the radial artery, or the saphenous vein. For patients with severe aortic calcification in whom the ascending aorta cannot be side-clamped for aortocoronary bypass, the GEA is a useful bypass conduit because it can be used as an in situ graft and does not require a proximal aortic anastomosis. Using the GEA and bilateral IMAs, complete revascularization with all-arterial in situ grafting can be accomplished: for example, RIMA-LAD, LIMA-circumflex artery, and GEA-RCA. This combination allows us to perform no-touch operations on the aorta.
Flow competition and graft narrowing are major concerns in GEA grafting [6, 20, 21]. Suma and coauthors [10] and Uchida and Kawaue [21] reported that a GEA graft anastomosed onto a coronary artery with less critical lesions often shows string signs as a result of competitive native flow. Flow competition and graft narrowing can lead to late graft occlusion. Of the 33 GEA occlusions (13 early and 20 late) in our study, eight (24.2%) showed flow competition with the native coronary artery or other grafts. Furthermore, in 8 of the 11 patients with string signs in the early angiographic study and 10 of the 15 with string signs in the late study, the string signs were also attributed to the flow competition mechanism. We intentionally do not anastomose the GEA to a mildly stenosed high-flow coronary artery. However, in some patients, the degree of native coronary stenosis was improved after CABG or the degree of stenosis was overestimated, and these phenomena are difficult to interpret on the basis of preoperative angiography. Uchida and Kawaue [12] analyzed the flow patterns of the GEA and the native coronary artery. They found that the frequency of GEA-dependent flow patterns, rather than native coronary-dependent flow patterns, increased as the degree of native coronary artery stenosis become more severe and as the location of the native coronary stenosis became more distal. They also pointed out that lesions resulting from a previous myocardial infarction require less blood flow than lesions that are due to angina. Flow competition with other high-flow bypass conduits can also occur if the GEA and saphenous vein grafts are placed in the same coronary system, such as a combination of GEA-posterior descending artery and saphenous vein-atrioventricular artery. If double bypass grafting is required for a single coronary system, a sequential graft should be considered.
Therefore, the optimal graft target of the in situ GEA is the RCA with severe proximal stenosis, the RCA with previous myocardial infarction, or the distal RCA, such as the right posterior descending artery or the atrioventricular artery. Sequential grafting with the GEA can be performed to the posterior descending artery, the atrioventricular artery, the posterolateral branch of the circumflex artery, or any combination of these. If revascularization of an RCA with high flow and mild stenosis is required, the saphenous vein should be chosen as the graft conduit because it can provide high distal flow. However, saphenous vein graft disease is of great concern and can develop eventually. Alternatively, the radial artery or the RIMA can be used, although the long-term patency rates of the radial artery are still under investigation and the in situ RIMA may not reach the distal RCA.
Early occlusion of the GEA immediately after CABG can be triggered by postoperative vasospasm. In this series, there was one case of GEA spasm, which resulted in postoperative myocardial infarction. Angiography demonstrated diffuse narrowing of the GEA on postoperative day 5, but it was found to be patent at repeat angiography 6 months after operation. The distal part of the GEA, especially at the anastomosis, is the most prone to vasospasm. The angiographic results should be interpreted carefully. Even though grade B anastomoses were found at angiography, we do not perform coronary intervention if the patient remains angina free. In our hospital, master double-equivalent exercise was performed by all patients prior to discharge whether or not angina had recurred. Of the 39 patients with grade B anastomoses found at early angiography, 17 underwent repeat angiography. Resolution of the anastomotic stenosis was observed in 5, graft occlusions resulting from progression of the stenosis was observed in 4, and in the other 8 patients, the degree of stenosis remained unchanged at repeated angiography. As prophylaxis for late graft spasm, oral administration of nicorandil or diltiazem hydrochloride should be maintained for at least 6 months after CABG in those who undergo GEA grafting.
The actuarial 1-year patency rate of the GEA in our survey was 98.7%, comparable to that of the IMAs (99.6%). However, the graft patency rate of the GEA dropped to 91.1% at 3 years and 84.4% at 5 years, which is substantially inferior to that of the LIMA (98.8% at 3 years and 97.0% at 5 years). Suma and colleagues [4, 19, 20] published a series of angiographic follow-up results of GEA grafting. In 1993, the early patency rate in 152 patients was 95% [6]. In 1996, the midterm patency rate in 400 patients with GEA grafting was 94% within 1 year and 94% at 2 to 5 years [19]. In 2000, late angiographic results including a total of 936 patients undergoing GEA grafting were published, and the patency rates decreased to 91.4% at 1 year and 80.5% at 5 years [20]. The reasons for the decrease in long-term graft patency rates were unclear. A nonfunctioning GEA graft anastomosed to high-flow vessels may play a part in inferior long-term angiographic results. Suma’s latest report [20] were comparable to our study.
Late graft occlusion of the GEA was observed more frequently than expected when we started to use the GEA 11 years ago. The late occlusions may increase the number of late cardiac-related events. Our angiographic study demonstrated that the graft patency rate of the GEA is inferior to that of the IMAs but similar to that of the saphenous vein. These differences in graft patency may be due to differences in the target coronary vessels and differences in the quality of the graft conduit. Saphenous vein graft disease is accelerated more than 5 years after CABG and may not be evident in a short observation period. The fate of the GEA graft is also unknown; thus, further angiographic long-term follow-up is necessary.
Although the graft patency rate of the GEA was inferior to that of the IMA, cardiac-related events were adequately prevented. The 5-year survival and event-free rates in this study were 92.6% and 84.2%, respectively. Isomura and associates [22] reported late data for patients who had received both a GEA graft and an IMA graft; the 7-year survival rate excluding noncardiac death was 96.8% and a cardiac-related event-free rate was 92.2%. Jegaden reported the long-term results of patients who underwent CABG using bilateral IMAs and the GEA, and the 4-year survival rate was 96.5%. Cardiac-related events can differ depending on the grafts used in combination with the GEA. The better cardiac-related event-free rate in our study may be due to the patent IMA-LAD grafts.
Our study involved a single surgical group, which may have biased the operative data. The majority of patients were referred from outside the hospital. Only 10% of the patients were followed up at our outpatient clinic; the others were followed up at local hospitals or by private cardiologists, and this difference might have influenced the late results. Repeat angiography was carried out in only 77 patients, and it was difficult to determine the fate of graft stenoses. The graft patency rate in each graft can be affected by the target vessels.
In summary, minimum adverse effects were noted after GEA grafting. We believe the GEA is ideal for revascularization of the distal RCA with severe proximal stenosis or proximal occlusion. The graft patency rate of the GEA was similar to that of the IMAs at early angiography, but it became inferior to IMA rates more than 3 years after CABG. The late cardiac-related events may be affected by late graft failure.
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