J
THoRAc CARDIOVASC SURG
1989;97:826-31
Coronary artery bypass grafting with the right gastroepiploic artery The excellent results of coronary artery bypass with the internal mammary artery and the increasing numbers of patients who need coronary reoperations, but for whom conventional bypass conduits are not available, have prompted us to evaluate alternative arterial bypass conduits. The right gastroepiploic artery has been used as a coronary bypass graft in 36 patients (32 men), whose ages ranged from 29 to 71 years. Twenty-two patients had had previous coronary bypass grafting and six of these were undergoing their third bypass operation. The right gastroepiploic artery was used as an in situ graft to the right coronary artery or circumflex branches for 17 patients and as an aorta-eoronary ("free") graft in 19 patients, six to the left anterior descending or diagonal, six to the circumflex, and seven to the right coronary artery. In conjunction with right gastroepiploic artery grafting, 16 patients 'received bilateral internal mammary artery grafts and 17 received one internal mammary artery graft. HistologicaUy, right gastroepiploic artery segments from 18 patients could not be distinguished from internal mammary artery segments, and no evidence of atherosclerosis was found. Two patients died in the hospital, one intraoperatively and one 3 months after the operation, of a perioperative stroke. Perioperative morbidity included wound complication in three and reexploration for bleeding in two. At late follow-up 1 to 38 months after operation, two late deaths had occurred and 21 patients were free of symptoms. Postoperative angiography (postoperative interval 1 week to 13 months) was performed in nine grafts, three in situ grafts to the right coronary artery and six free grafts that included two to the left anterior descending, three to the circumflex, and one to the right coronary artery. AU right gastroepiploic artery grafts were patent. The right gastroepiploic artery is an arterial conduit that can be used as an in situ graft to posterior coronary vessels and as a free graft to any coronary arterial system. Early graft patency has been excellent, and the histologic similarity between the right gastroepiploic artery and the internal .nammary artery suggest that the long-term results will be favorable.
Bruce W. Lytle, MD, Delos M. Cosgrove, MD, Norman B. Ratliff, MD, and Floyd D. Loop, MD, Cleveland, Ohio
h e long-term success of coronary artery bypass with the internal mammary artery (IMA),,2 and the increasing numbers of patients who are candidates for coronary reoperations but who lack suitable bypass conduits are factors promoting the evaluation of alternative arterial coronary bypass conduits. Surgeons need another IMA. In the formative years of the myocardial revascularization era, the right gastroepiploic artery was used by Bailey and associates-:' and Fitzgibbon, Hooper, and Maclver' for Vineberg-type myocardial implantation.
From the Department of Thoracic and Cardiovascular Surgery, The Cleveland Clinic Foundation, Cleveland, Ohio. Received for publication July 8, 1988. Accepted for publication Nov. 3, 1988. Address for reprints: Bruce W. Lytle, MD, Department of Thoracic and Cardiovascular Surgery, The Cleveland Clinic Foundation, One Clinic Center, 9500 Euclid Ave., Cleveland, OH 44195.
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However, Pym and colleagues" were the first to report the use of this conduit for direct coronary anastomoses when they described in situ right gastroepiploic grafts to the right coronary artery and posterior circumflex branches." Carter? used in situ right gastroepiploic grafts to revascularize posterior coronary arteries, and Suma, Fukumoto, and Takeuchi" have employed the vessel as an in situ graft to the anterior descending coronary artery. This report describes our experience with the use of the right gastroepiploic artery as an in situ or "free" (aorta-coronary) coronary bypass graft in 36 patients from 1985 through 1988. Patients and methods Patient population.Thirty-six patients (32 men and four women), whose ages ranged from 29 to 71 years (mean age 51 years), have received coronary bypass grafts performed with the right gastroepiploic artery between July 1985 and May 1988. Preoperative catheterization showed that 30 patients
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Fig. 1. Staple gun used to divide the omental branches of the right gastroepiploic artery. had 50% stenosis or greater in three coronary arteries, five in two arteries, and one in a single artery; four patients had stenosis of the left main coronary artery, as well. Left ventricular function, determined angiographically, was normal in 14 patients, mildly impaired in 13, moderately impaired in three, and severely impaired in six. Thirty-two patients had chronic symptoms of angina, two had symptoms of congestive heart failure, and 27 had had previous myocardial infarction. Preoperative symptom status was New York Heart Association (NYHA) functional class I in one patient, II in 12, III in 10, and IV in 12 patients. Twenty-two patients had had a previous bypass operation and six had had two previous bypass operations. Six patients had undergone previous saphenous vein stripping for reasons other than the use of vein for arterial bypass conduits. Ten patients had had a previous abdominal operation, including appendectomy, nine patients, hysterectomy, two, colon polypectomy, one, and cholecystectomy, one patient. Indications for the use of the right gastroepiploic artery for patients who still had saphenous vein available were hyperlipidemia, previous vein graft failure, unfavorable-looking saphenous vein, and combinations of those indications. Procedure. The median sternotomy is performed and the incision in the midline abdominaLfascia is extended to a point just above the umbilicus. Simultaneous preparation of the right gastroepiploic artery and IMA dissection is usually possible. After the peritoneal cavity has been entered, the right gastroepiploic artery is identified on the greater curvature of the stomach and branches to the omentum are divided with a staple gun (Fig. 1). Branches to the stomach are ligated with 4-0 silk ties (Fig. 2). The right gastroepiploic artery is isolated from the point on the greater curvature of the stomach where it becomes less than 1 mm in diameter back to the level of the pylorus,just distal to its origin from the gastroduodenal artery. The patient is then given heparin and arterial and venous cannulation is accomplished. If the operative plan is to use the right gastroepiploic artery as an in situ graft, the vessel is divided distally and flow assessed. The diaphragmatic surface of the heart is then dissected from the diaphragm and a judgment made as to the
Fig. 2. Branches to the stomach are divided with clamps and ties and the gastroepiploic pedicle is isolated proximal to its origin from the gastroduodenal artery.
probable location for grafting the right coronary artery. If a posterolateral branch of the right coronary artery is to be grafted, the right gastroepiploic artery is usually routed posterior to the stomach, through the omental bursa (lesser sac), through the divided lesser omentum, and through a cruciate hole in the diaphragm (Fig. 3), which is exposed by dividing the left triangular ligament of the liver. This retrogastric position of the right gastroepiploic artery can also be used for grafting posterolateral circumflex branches and the posterior descending branch of the right coronary artery. The main right coronary artery can be grafted through a retrogastric approach by placing the heel of the anastomosis distally on the right coronary artery and extending the toe of the anastomosis proximally. However, when the posterior descending coronary artery or the main right coronary artery is to be grafted, the right gastroepiploic artery is usually routed anterior to the stomach and the liver (Fig. 4). When the right gastroepiploic artery is used as an in situ graft, the diameter of the anastomotic end is usually about 1.25 mm. We have not used the right gastroepiploic artery as an in situ graft to the left anterior descending coronary artery. Our strategy for grafting anterior left-sided vessels has been to perform a free (aortacoronary) graft. When a free graft is planned, the right gastroepiploic artery is divided at both the distal and proximal ends. After cardiopulmonary bypass has been commenced, the aorta is crossclamped and cardioplegia is used to establish cardiac arrest. The distal anastomoses of the right gastroepiploic artery grafts are completed with an interrupted 7-0 silk technique. Proximal anastomoses of free right gastroepiploic grafts are accomplished with an interrupted 7-0 or 6-0 silk suture technique. When free grafts are performed as part of a primary operation, the gastroepiploic artery can often be anastomosed directly to the ascending aorta, but during
The Journal of Thoracic and Cardiovascular Surgery
8 28 Lytle et al.
(
.~
.
,
Fig. 3. The retrogastric route is usually the mostdirect when
distal right coronary arteries are to be grafted with an in situ right gastroepiploic artery graft. reoperations the proximal anastomosis is constructed either to the hood of an old vein graft or to a short segment of saphenous vein sewn to the aorta. The thickening of the reoperative aorta makes the proximal anastomosis of a free right gastroepiploic artery graft directly to the aorta difficult. Results Perioperative results. All patients received a single right gastroepiploic artery graft, 17 that were in situ grafts and 19 that were free grafts. The coronary vessels grafted with in situ right gastroepiploic artery grafts were the main right coronary artery in three patients, the distal right coronary artery branches (posterior descending or posterolateral) in 12, and the posterolateral circumflex branches in two patients. Free right gastroepiploic artery grafts were used to the anterior descending or diagonal branch in six patients, the circumflex artery in six, the main right coronary artery in five, and the distal right coronary branches in two patients. The number of total grafts (distal anastomoses) that patients received was one graft in one patient, two in 11
Fig. 4. The antegastric route into the pericardium is used when the main right coronary artery is to be grafted. Other authors have used this approach to graft the left anterior descending coronary artery.
patients, three in 14 patients, and four grafts in 10 patients. Sixteen patients received bilateral IMA grafts at the same operation and 17 received a single IMA graft. Three patients received sequential IMA grafts. Sixteen patients received saphenous vein grafts in addition to arterial grafts, and one patient underwent resection of a left ventricular aneurysm. Two in-hospital deaths occurred, one from a myocardial infarction (not in the distribution of the gastroepiploic graft) at emergency operation for evolvingmyocardial infarction, and one 3 months after operation from complications of a perioperative stroke. One nonfatal perioperative myocardial infarction occurred (not in the distribution of the gastroepiploic graft). Two patients underwent reexploration for postoperative bleeding. Three patients had wound complications, two of which were major sternal wound complications that necessitated reoperation. Both patients had diabetes and had received bilateral IMA grafts. One patient had a superficial wound separation in the abdominal portion of the incision, which healed with conservative treatment. The postoperative in-hospital stay ranged from 7 to 126
Volume 97 Number 6 June 1989
days (mean 17 days); of the 34 in-hospital survivors, 12 (nine of whom were undergoing reoperation) stayed in the hospital more than 10 postoperative days. Distal segments of the right gastroepiploic artery from 18 patients were examined histologically. None of the segments exhibited atherosclerosis, and they were histologically indistinguishable from segments of IMAs. Late results. Follow-up of the late survivors is complete at a range of 1 to 34 months after operation . Two patients have died, one patient 5 months after operation from complications of diverticulitis and one of congestive heart failure 14 months after the operation. Functional class (NYHA) at follow-up was I in 21 patients, II in eight, and III in one patient; no patient was in class IV after the operation. Angiograms of nine right gastroepiploic artery grafts have been obtained at postoperative intervals ranging from 1 week to 13 months-three in situ grafts to the right coronary system (Fig. 5), three free grafts to the circumflex system, two free grafts to the left anterior descending system (Fig. 6), and one free graft to the right coronary artery. All right gastroepiploic artery grafts were patent. In those nine patients, nine IMA grafts were also studied, and all were patent. In addition, eight saphenous vein grafts were studied, of which four were occluded. Discussion Since the dawn of the era of myocardial revascularization, the concept of arterial grafting has been appealing to surgeons. Vineberg's technique? of intramyocardial implantation of the IMA demonstrated that this artery could remain patent despite limited outflow, although the results of implantation were unpredictable. Arterial implantation was extended to include placement of the right gastroepiploic artery into the posterior myocardium by Bailey and associates'" and Fitzgibbon , Hooper, and Maclver,' and patency was documented angiographically in four patients within a year after operation. The advent of coronary artery bypass grafting with the saphenous vein and the obvious efficacy of techniques involving the direct anastomoses of grafts to the coronary arteries superseded the strategy of arterial implantation. However, although surgeons made the conceptual conversion from implantation to bypass grafting techniques with the IMA, the right gastroepiploic artery was not used for direct revascularization until Pym and colleagues" reactivated its use and Carter' and Suma, Fukumoto, and Takeuchi" followed suit. Other arteries have also been used for coronary. bypass grafting . Edwards and associates and Mueller,
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Fig. 5. Celiac opacification showing patency of an in situ right gastroepiploic artery graft to the right coronary system 3
weeks after operation. Lewis, and Edwards I I used the splenic artery as an in situ graft to the right coronary artery and reported postoperative patency in five of six such grafts studied. However, the laborious procedure required to harvest the splenic artery and the high prevalence of atherosclerosis in that vessel have stifled the popularity of that technique. Segments of radial artery have been used as free (aorta-coronary) grafts , but patency rates of those grafts have not been favorable. " The superiority of the long-term results of IMA grafting compared with those of saphenous vein grafting is now a matter of record and has led to the dramatic expansion of the use of the IMA for bypass grafting. The hope that the long-term performance of right gastroepiploic artery--coronary artery bypass grafts will mimic that of IMA grafts is one factor leading to renewed interest in this artery. Other factors promoting the use of the right gastroepiploic artery are the increasing population of patients who are candidates for coronary bypass grafting, but whose standard bypass conduits are not available, usually because of a previous operation , and the dismal record of other alternative coronary bypass grafts , such as upper extremity vein, homologous vein grafts, umbilical vein, and prosthetic grafts. 13·1 5 There are similarities between the IMA and the right gastroepiploic artery that allow the speculation that the long-term results of bypass grafts with these vessels may be similar. They are approximately the same size, both arteries in situ are straight vessels with little tortuosity, and they give off multiple branches. Our data and studies by others have shown that the IMA and the gastroepiploic artery are histologically similar and that
8 3 a Lytle et al.
The Journal of Thoracic and Cardiovascular Surgery
Fig. 6. A patent free right gastroepiploic graft to the left anterior descending coronary artery 1 week after operation.
atherosclerosis intrinsic to either vessel is uncommon. 16• 17 The use of the right gastroepiploic artery for coronary bypass grafting has not produced many perioperative complications. Neither of the two perioperative myocardial infarctions that occurred was in the distribution subtended by the gastroepiploic grafts . None of our patients had any major in-hospital abdominal complications. Two major wound complications did occur, but they involved the sternal portion of the wound in diabetic patients who were also undergoing bilateral IMA grafting. On the other hand, use of the right gastroepiploic artery does make the operative procedure more complex, and the possibility must be considered that the addition of a laparotomy to hundreds of coronary bypass operations might lead to some increase in perioperative morbidity. Twelve patients required hospitalization for more than 10 postoperative days, whereas the standard postoperative in-hospital stay at our institution is 7 days. However, nine of those patients had undergone reoperation. We have used the right gastroepiploic artery both as an in situ graft and as an aorta-coronary free graft. As an in situ graft the right gastroepiploic will usually reach branches of the right coronary artery and posterior circumflex branches . Suma, Fukumoto, and Takeuchi" measured the angiographic size of right gastroepiploic arteries and concluded that the diameter of this vessel was greater than 1.5 mm in 96 of 100 cases. However,
we have found that, when the right gastroepiploic artery is used as an in situ graft to distal branches of the right coronary system, the diameter of the distal end where the anastomosis is constructed to the coronary vessel is usually between 1.25 and 1.5 mm, about the size of a small IMA. The proximal right gastroepiploic artery is a large vessel, equivalent in size to most IMAs, but as it extends distally it appears to get smaller faster than the IMA does. Our experience with free IMA grafts has been favorable," and we have extended this strategy to the right gastroepiploic artery. Use of the right gastroepiploic artery as a free graft increases the versatility of this conduit. Angiographic studies have indicated a low prevalence of obstructive lesions intrinsic to the right gastroepiploic artery," but when it is used as an in situ graft the possibility exists that it could be jeopardized by aort ic or celiac atherosclerosis, a problem that is avoided with free grafts . The difficulty with free grafts is the proximal anastomosis, which is technically demanding. The crucial issue for gastroepiploic artery grafts is the documentation of patency rates. So far, the postoperative angiographic assessment of these grafts has been extremely encouraging. All nine grafts that we have restudied by direct angiography have been patent, including six free grafts. In the published series of Pym and associates," all six in situ grafts studied with celiac opacification were patent, and since that publication date they have documented patency in eight further
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Number 6 June 1989
grafts (personal communication). Suma, Fukumoto, and Takeuchi' studied two grafts and both were patent. In Black and Gibbon's series," nine in situ grafts were studied, some with subselective gastroepiploic angiograms, and seven were patent. However, none of these arteriograms has been performed more than 2 years after operation, and to have real appeal the gastroepiploic artery must have a longevity approaching that of the IMA. Our indications for the use of the right gastroepiploic--coronary artery graft are in evolution. We currently use the right gastroepiploic artery as the bypass conduit of choice after the IMAs and lower extremity veins have been exhausted. However, our initial favorable experience has persuaded us to liberalize the indications for its use, and we now perform gastroepiploic grafts in some situations in which lower extremity vein is still available: for example, young patients with hyperlipidemia, a subset of patients known to have poor long-term vein graft patency 20; patients with saphenous vein that is available but is of poor quality; and patients undergoing reoperation for vein graft failure. The use of the right gastroepiploic artery increases the difficulty of operation for coronary bypass. However, if the early promise of right gastroepiploic grafts is fulfilled, with the demonstration of IMA-type long-term results, this procedure will become common and will represent another factor increasing the complexity of coronary bypass operations with the goal of improving the long-term results. REFERENCES 1. Lytle BW. Loop FD, Cosgrove DM, Ratliff NB, Easley K, Taylor Pc. Long-term (5 to 12 years) serial studies of internal mammary artery and saphenous vein coronary bypass grafts. J THORAC CARDIOVASC SURG 1985;89:24858. 2. Loop FD, Lytle BW, Cosgrove OM, et al. Influence of the internal mammary artery graft on 10-year survival and other cardiac events. N Engl J Med 1986;314:1-6. 3. Bailey CP, Hirose T, Aventura A, et al. Revascularization of the ischemic posterior' myocardium. Chest 1967; 52:273-85. 4. Bailey CP, Hirose T, Brancato R, Aventura A, Yamamoto N. Revascularization of the posterior (diaphragmatic) portion of the heart. Ann Thorac Surg 1966;2:791-805. 5. Fitzgibbon GM, Hooper 0, Maciver DA. Vineberg operation for myocardial ischemia without angina: a preliminary report. Can J Surg 1970;13:135-43.
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6. Pym J, Brown PM, Charrette EJP, Parker JO, West RO. Gastroepiploic-coronary anastomosis: a viable alternative bypass graft. J THORAC CARDIOVASC SURG 1987;94: 256-9. 7. Carter MJ. The use of the right gastroepiploic artery in coronary artery bypass grafting. Aust NZ J Surg 1987; 57:317-21. 8. Suma H, Fukumoto H, Takeuchi A. Coronary artery bypass grafting by utilizing in situ right gastroepiploic artery: basic study and clinical application. Ann Thorac Surg 1987;44:394-7. 9. Vineberg AM. Development of anastomosis between coronary vessels and transplanted internal mammary artery. Can Moo J 1946;55:117-9. 10. Edwards WS, Lewis CE, Blakeley WR, Napolitano L. Coronary artery bypass with internal mammary artery and splenic artery grafts. Ann Thorac Surg 1973;15: 35-9. I I. Mueller CF, Lewis CE, Edwards WS. The angiographic appearance of splenic-to-coronary artery anastomosis. Radiology 1973;106:513-6. 12. Fisk RL, Brooks CH, Callaghan JC, Dvorkin J. Experience with the radial artery graft for coronary artery bypass. Ann Thorac Surg 1976;21:513. 13. Stoney WS, Alford WC Jr, Burrns GA, et al. The fate of arm veins used for aorta-coronary bypass grafts. J THORAC CARDIOVASC SURG 1984;88:522-6. 14. Bical 0, Brachet J, Laurian C, et al. Aortocoronary bypass with homologous saphenous vein: long-term results. Ann Thorac Surg 1980;30:550-7. 15. Sapsford RN, Oakley GO, Talbot S. Early and late patency of expanded polytetrafluoroethylene vascular grafts in aorta-coronary bypass. J THORAC CARDIOVASC SURG 1981;81:860-4. 16. Kay HR, Korns ME, Flemma RJ, Tector A, Lepley D. Atherosclerosis of the internal mammary artery. Ann Thorac Surg 1976;21:504-7. 17. Larsen E, Johansen A, Anderson D. Gastric arteriosclerosis in elderly people. Scand J Gastroenterol 1969;4: 387-9. 18. Loop FD, Lytle BW, Cosgrove OM, Golding LAR, Taylor PC, Stewart RW. Free (aorta-coronary) internal mammary artery grafts. J THORAC CARDIOVASC SURG 1986;92:827-31. 19. Black AJR, Gibbons F. Angiographic visualization of a right gastroepiploic artery-left circumflex coronary artery graft. Cathet Cardiovasc Diag 1987;13:121-4. 20. Lytle BW, Kramer JR, Golding IR, et al. Young adults with coronary atherosclerosis: 10-year results of surgical myocardial revascularization. J Am Coli Cardiol 1984; 4:445-53.