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1 Limited Flow Capacity of the Right Gastroepiploic Artery Graft: Postoperative Echocardiographic and Angiographic Evaluation Masami Ochi, MD, Nobuo Hatori, MD, PhD, Masahiro Fujii, MD, Yoshiaki Saji, MD, Shigeo Tanaka, MD, and Hiroshi Honma, MD Department of Surgery II, Division of Cardiovascular Surgery, and Department of Internal Medicine I, Nippon Medical School, Tokyo, Japan It has been more than 10 years since the first clinical application of the right gastroepiploic artery (GEA) as an in situ graft to the coronary artery was performed [1 4]. The GEA has been used enthusiastically with much expectation from the cardiac surgeons as the next alternative to the internal thoracic artery (ITA) [5 8]. The GEA has a wide individual variation in its length and caliber. However, there has been little data presented providing criteria for the usage of this artery with regard to the characteristics of the flow capacity of the GEA. We assessed the flow capacity of the GEA by analyzing the results of the postoperative angiographic and dobutamine stress echocardiographic evaluations in patients who underwent coronary artery bypass grafting using both the GEA and the ITA. Material and Methods Thirty patients who underwent isolated coronary artery bypass grafting using both the ITAs and GEA with or without venous grafts were studied. There were 24 men and all had multivessel coronary lesions. Their age ranged from 48 to 72 years with a mean age of 61.2 years. None of the patients experienced angina during daily life, or received antianginal drugs postoperatively. The number of bypassed vessels was two to six (mean, 3.8). The left anterior descending artery was revascularized by the left ITA in all patients. The GEA was grafted to the Accepted for publication Nov 28, Address reprint requests to Dr Ochi, Sendagi Bunkyo-ku, Tokyo, , Japan; ochi/surg2@nms.ac.jp. Background. The flow capacity of the right gastroepiploic artery graft has not been clarified. Methods. Angiographic and echocardiographic studies were conducted in 30 patients who had undergone coronary artery bypass grafting using both the internal thoracic and right gastroepiploic arteries. The luminal diameter of the arterial grafts was measured from the postoperative angiograms. The adequacy of the myocardial blood supply from the arterial grafts was evaluated by dobutamine stress echocardiography. Results. With echocardiography, 14 patients exhibited an ischemic response in the gastroepiploic artery grafted region, whereas no patients exhibited an ischemic response in the internal thoracic artery grafted area. The luminal diameter of the gastroepiploic artery and a younger age were correlated with the ischemic response observed in the dobutamine stress echocardiography. A luminal diameter of the gastroepiploic artery of greater than 2.6 mm had the highest sensitivity and specificity for a nonischemic change. Conclusions. To generate the maximal flow reserve, the luminal diameter of the gastroepiploic artery when used as a graft should be sufficiently large enough, nearly 3 mm at the anastomosis. (Ann Thorac Surg 2001;71:1210 4) 2001 by The Society of Thoracic Surgeons right coronary artery, which had critical occlusive lesions at its proximal segment with or without distal lesions, or to the distal branch of the dominant left circumflex artery, which had a significant area of perfusion. The GEAs that were grafted to an isolated small branch were not included in this study. Sequential anastomoses were performed with the left ITA in 17 patients and with the GEA in 11 patients (Table 1). Because preoperative angiograms of the GEA can be obtained during diagnostic catheterization by the cardiologists, it has been our standard procedure to use a GEA with a luminal diameter of greater than 2 mm at the presumptive point of anastomosis on the angiogram. The GEA was brought into the pericardial cavity anterior to the stomach and liver. All patients were operated on by a single surgeon (MO). An angiographic examination was performed from 3 to 21 months (mean, 6.8 months) postoperatively as a routine practice to confirm the status of the grafts, as well as that of the coronary arteries. All patients were informed of this preoperatively and all accepted to comply with the procedure. During the same period, all patients were offered the option of dobutamine stress echocardiography (DSE) to document the adequacy of the myocardial blood flow, and informed consent was obtained. Protocol of the Postoperative Dobutamine Stress Echocardiography Study The protocol for the DSE [9] included infusion of nitroglycerin at 0.1 to 0.2 g kg 1 min 1, followed by 2001 by The Society of Thoracic Surgeons /01/$20.00 Published by Elsevier Science Inc PII S (00)

2 Ann Thorac Surg OCHI ET AL 2001;71: GEA AND DSE 1211 Table 1. Graft Placement Graft LCA RCA LAD Diag. OM PL Prox. PD AV Sequential Graft LITA RITA 4 1 GEA SVG AV atrioventricular branch; Diag. diagonal branch; LAD left anterior descending artery; LCA left coronary artery; OM obtuse marginal branch; PD posterior descending artery; Prox. proximal segment; PL posterolateral branch; RCA right coronary artery. infusion of dobutamine at 4 g kg 1 min 1 with stepwise increases to 8, 12, 16, 20, 25, and 30 g kg 1 min 1 (infusion at each dose for 3 minutes). The electrocardiogram was monitored continuously, and the blood pressure, 12-lead electrocardiogram, and echocardiogram were recorded at baseline and at the end of each stage. The following end points were applied to the DSE: (1) appearance of a new regional wall motion abnormality involving two or more wall segments; (2) attaining 85% of the target heart rate; (3) an ST-segment depression or elevation greater than 2 mm; (4) occurrence of significant chest pain; (5) an increase in the systolic blood pressure more than 200 mm Hg; (6) a decrease in the systolic blood pressure of 20 mm Hg or to less than 90 mm Hg; (7) appearance of complex ventricular arrhythmias; and (8) administration of the maximum dose of dobutamine. Echocardiographic images were video-recorded and reviewed by at least two experienced cardiologists. The presence of an ischemic response to the DSE was diagnosed when one of the following involving two or more wall segments was identified: (1) development of asynergy in the patients without a wall motion abnormality at rest and (2) worsening of the wall motion abnormality in the patients with a wall motion abnormality at rest (ie, deterioration from hypokinesis to akinesis or dyskinesis). Angiographic Examination Diagnostic angiographic catheters (5F) of various shapes were used through a transfemoral approach in all patients. All grafts were investigated for patency. The ITAs and GEAs were visualized selectively or semiselectively. Care was taken to obtain a cineangiogram in which both the distal segments of the arterial grafts around the anastomosis and the catheter could be seen in the same frame. Coronary angiograms were also obtained. Before angiography, a 2.5-mg bolus of isosorbide dinitrate was injected into the coronary arteries and arterial grafts to eliminate spasms. The luminal diameter of the arterial grafts near the anastomosis was measured from the angiogram by comparing it with the lumen of a 5F angiographic catheter (1.67 mm) by means of computer-analyzed Quantitative Coronary Angiography (Cardio 500, KONTRON Elektronik GmbH, Munich, Germany). The angiographic status of the arterial grafts was evaluated by classifying the pattern of the blood flow of the grafted coronary artery by the arterial graft as follows: 1. A dominant graft was defined when the coronary artery was visualized only or mainly by the graft injection. 2. A balanced condition was defined when the coronary artery was equally visualized either by the graft or by the intracoronary injection. 3. A dominant coronary artery was defined when the coronary artery was entirely visualized by the intracoronary injection and not by the graft. Statistical Analysis Statistical analysis was performed using SPSS10.0J (SPSS Inc, Chicago, IL). The distributions were analyzed by the Kolmogorov-Smirnov test and the variances of the data by the Levene test. Then, comparisons between the two groups were performed using the unpaired Student s t test. The 2 test using the Fisher s direct method was used for comparison of categoric data. A multivariate logistic regression analysis was performed using the patient characteristics and the difference between the ischemic and nonischemic changes in the GEA anastomosed region as independent covariates, by selecting a forward-stepping selection method with maximum likelihood estimates and default criteria. A receiver operator characteristic curve was used to optimize the sensitivity and specificity of using the diameter of the GEA to predict nonischemic change. Data were presented as mean standard deviation. All p values were two-tailed, and a p value of less than 0.05 was considered significant. Results Angiography The ITAs, as well as the GEAs, were patent and appeared normal in all patients. The luminal diameter of the ITAs ranged from 1.4 to 3.1 mm ( mm) and that of the GEA from 1.5 to 4.5 mm ( mm), and the latter was significantly larger than the former (p 0.005). The status of the ITAs was: A dominant ITA in 19 patients, balanced condition in 7, and dominant coronary in 4 patients. The status of the GEAs was: A dominant GEA in 23 patients, balanced condition in 6, and dominant coronary in 1 patient. Residual nongrafted vessels in the right coronary system were identified in 5 patients. Dobutamine Stress Echocardiography In the DSE, no patients exhibited new wall motion abnormalities in the anteroseptal to lateral region where the ITAs were grafted. On the contrary, a new wall motion abnormality during the DSE was identified in 14 patients in the inferoposterior region where the GEA was anastomosed. Among these patients, 3 complained of chest pain with an ST-segment depression on the electrocardiogram during the DSE. Patients were divided into three groups according to

3 1212 OCHI ET AL Ann Thorac Surg GEA AND DSE 2001;71: Table 2. Groups of Patients According to the Presence of Ischemic Change in the DSE and Residual Nongrafted Vessels in the GEA-Grafted Region Variables Group I Group II Group III Patients Ischemic change in DSE ( ) ( ) ( ) Residual nongrafted vessels ( ) ( ) ( ) DSE dobutamine stress echocardiography; artery. GEA gastroepiploic the results of the DSE and the presence of residual nongrafted vessels in the inferoposterior region on the angiogram (Table 2). Group I patients did not exhibit an ischemic change in the DSE and did not have residual nongrafted vessels in the inferoposterior region (N 16). Group II patients exhibited an ischemic change in the DSE, but did not have residual nongrafted vessels in the inferoposterior region (N 9). Group III patients exhibited an ischemic change in the DSE and had residual nongrafted vessels in the inferoposterior region (N 5). The luminal diameter and angiographic status of the arterial grafts of the GEA in each group are shown in Tables 3 and 4. All patients in group III exhibited satisfactory angiographic results and had GEAs with a luminal diameter greater than 3 mm. The presence of residual nongrafted vessels in the right coronary system, however, made it difficult to determine the adequacy of flow reserve of the GEA. Accordingly, patients in groups I and II were analyzed for predictors of the ischemic change in the DSE. On univariate analyses, the age, body surface area, presence of hypertension, diabetes or hyperlipidemia, and history of smoking, or old myocardial infarction were not associated with an ischemic change. The variables observed during the DSE also were not associated with an ischemic change in the DSE. The only significant variable associated with an ischemic change was the luminal diameter of the GEA (Fig 1). A multivariate logistic regression analysis was performed to identify the independent predictors for the ischemic change in the GEA region. The results demonstrated that the luminal diameter of the GEA and a younger age of the patients were significant independent predictors for the ischemic change. When the presence of hyperlipidemia was combined with these predictors, a much greater likelihood of the occurrence of an ischemic change in the GEA grafted region was obtained (Table 5). The receiver operator characteristic curve showed that a luminal diameter of the GEA of greater than 2.6 mm had a sensitivity of 70% and a specificity of 78.0% for nonischemic change in the GEA anastomosed region (Fig 2). Table 3. Mean Luminal Diameter of the ITAs and GEAs Artery Group I Group II Group III All Patients ITAs (mm) GEAs (mm) ITA internal thoracic artery; Table 4. Angiographic Status of the GEAs and Grafted Coronary Arteries Variable Group I Group II Group III GEA Dominant GEA Balanced Dominant coronary 1 GEA grafted vessel Totally occluded Not occluded Comment From the beginning of the development of the GEA as a graft to the coronary artery, its angiographic and anatomic relevancy has been confirmed by various investigations [10 13]. In addition, many aspects of the differences between the ITA and the GEA have been pointed out [14 19]. In the current study, ischemic wall motion abnormalities occurred in the DSE only in the region perfused by the GEA, even in the patients who exhibited acceptable angiographic findings for the GEA. Among the 9 patients in group II, 6 exhibited a definite angiographic dominancy of the GEA over the coronary artery. Furthermore, no wall motion abnormalities were induced in the DSE in the region perfused by the ITA. These results led us to assume that the flow capacity is apparently different between the GEA and ITA, especially under certain stress conditions. There have been several reports on the free flow rate and the diameter of the GEA for the anastomosis measured intraoperatively [6, 18, 20, 21]. A large luminal diameter correlated with better flow rates. None of the previous reports, however, have demonstrated the adequacy of the flow capacity of the GEA under maximum stress conditions. The results in this study clearly indicate that the luminal diameter of the GEA should be large enough (2.6 mm or more) to meet the myocardial oxygen demand during exercise. Many reports have warned that a GEA with a small diameter should not be anastomosed to a noncritically stenosed coronary artery because of the frequent occurrence of competitive flow between the coronary artery [8, 22 24]. As mentioned previously, 6 patients in group II showed angiographic dominancy (Fig 3). In 4 of these patients, the GEA grafted coronary artery was totally occluded. Dominant GEAs were supposed to perfuse the entire vascular bed of the grafted coronary artery. The response of grafts to increased blood flow under conditions of stress is correlated to the coronary vascular bed. The larger the grafted vascular bed, the more blood flow is required. The GEAs of small diameter may not be capable of supplying the entire coronary vascular bed with sufficient blood flow. The dominancy on the angiogram is one thing and the flow reserve of the GEA is another. The length of the GEA graft may influence its flow reserve. The distal segment of the GEA contains more

4 Ann Thorac Surg OCHI ET AL 2001;71: GEA AND DSE 1213 Fig 1. Luminal diameter of the gastroepiploic arteries of the patients in group I and group II. Patients 1 through 16 are included in group I, and patients 17 through 25 are in group II. smooth muscle cells and is smaller in diameter. Therefore, the distal segment of the GEA graft should be trimmed, because the distal segment of the arterial grafts is reactive and functions as a flow regulator [25]. Use of a shorter GEA graft has been advocated to obtain better blood flow [20]. However, the GEA has a wide individual variation in its length and caliber. In our series, 7 patients with a sequential graft of the GEA were included in the nonischemic group. Despite the need for a longer length of the GEA than that for nonsequential grafts, all these patients had GEAs with a luminal diameter of more than 3 mm. This indicates that the major determinant of the flow capacity of the GEA is its luminal diameter. As long as the luminal diameter of the GEA is large enough, the length of the GEA graft may not influence its flow reserve. Conversely, even if the length of the GEA is sufficient, a small luminal diameter is a contraindication to its use. There was at least one residual nongrafted vessel of the right coronary artery in the group III patients. All the patients in group III had GEAs with a luminal diameter of more than 3 mm (range, 3.1 to 3.8 mm; mean, 3.6 mm). In 4 of these patients, the GEA graft was anastomosed to the totally occluded right coronary artery. Whether the ischemic change was the result of the inadequate flow reserve of the GEA or the nongrafted vessels remained ambiguous. However, even in group II patients, there was 1 patient whose GEA was 3.3 mm in diameter (Fig 1). The right coronary artery of this patient was totally occluded at the proximal segment and the remainder of it was perfused by the GEA. A possibility still exists that the ischemic response in the group III patients was attributable to the inadequate flow capacity of the GEA. There may be other factors that influence the flow capacity of the GEA as a graft [19]. Further study, for example, a measurement of the change in the flow velocity of the GEA under stress conditions using transcutaneous Doppler echocardiography [26], may give us a solution to this problem. A possible explanation for why a younger age is an independent predictor for ischemic change in the DSE is an age-related reduction in the basal metabolic rate that reduces oxygen consumption of the heart [27, 28]. Aging is associated with a progressive loss of myocytes and an increase in the rate of degenerative change [29]. The Table 5. Multivariate Analysis for Ischemic Change in GEA-Grafted Region Variable Odds Ratio 95% CI p Value GEA diameter Age Hyperlipidemia Fig 2. Receiver operator characteristic curve showing a luminal diameter of the GEA of greater than 2.6 mm (*) had a sensitivity of 70% and a specificity of 78.0% for nonischemic change in the dobutamine stress echocardiography in the gastroepiploic arterygrafted region.

5 1214 OCHI ET AL Ann Thorac Surg GEA AND DSE 2001;71: Fig 3. A 62-year-old male patient in group II showing a dominant gastroepiploic artery with a luminal diameter of 2.5 mm. The entire right coronary artery is opacified by the gastroepiploic artery. structural and functional changes can affect the oxygen utilization of the heart. In conclusion, considering the high occurrence of ischemic change in the GEA grafted region, which is not observed at all in the ITA grafted region, the flow capacity of the GEA differs from that of the ITA especially under maximal stress conditions. In that sense, the GEA should not be used routinely in the same way as the ITA. The luminal diameter of the GEA as a graft to the coronary artery should be more than 2.6 mm at the anastomosis, and adding the thickness of the arterial wall, the outer diameter should be 3 mm or more. We are grateful to John Martin for his assistance in preparing the manuscript. References 1. 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: Pym J, Brown PM, Charrette EJP, Parker JO, West RO. Gastroepiploic-coronary anastomosis. A viable alternative bypass graft. J Thorac Cardiovasc Surg 1987;94: Suma H, Wanibuchi Y, Terada Y, Fukuda S, Takayama T, Furuta S. The right gastroepiploic artery graft. Clinical and angiographic midterm results in 200 patients. J Thorac Cardiovasc Surg 1993;105: Pym J, Brown PM, Pearson M, Parker J. Right gastroepiploicto-coronary bypass. The first decade of use. Circulation 1995;92(Suppl 2): Lytle BW, Cosgrove DM, Ratliff NB, Loop FD. Coronary artery bypass grafting with the right gastroepiploic artery. J Thorac Cardiovasc Surg 1989;97: Mills NL, Hockmuth DR, Everson CT, Robart CC. Right gastroepiploic artery used for coronary artery bypass grafting. J Thorac Cardiovasc Surg 1993;106: Grandjean JG, Boonstra PW, den Heyer P, Ebels TE. Arterial revascularization with the right gastroepiploic artery and internal mammary arteries in 300 patients. J Thorac Cardiovasc Surg 1994;107: Jegarden O, Eker A, Montagna P, et al. Technical aspects and late functional results of gastroepiploic bypass grafting (400 cases). Eur J Cardiothorac Surg 1995;9: Kishida H, Kusama Y, Homma H. Dobutamine stress echocardiography for the detection of coronary artery disease and viable myocardium. Jpn Heart J 1997;38: Suma H, Wanibuchi Y, Furuta S, Isshiki T, Yamaguchi T, Takanashi R. Comparative study between the gastroepiploic and the internal thoracic artery as a coronary bypass graft. Size, flow, patency, histology. Eur J Cardiothorac Surg 1991; 5: Van Son JAM, Smedts FM, Yang C-Q, et al. Morphometric study of the right gastroepiploic and inferior epigastric arteries. Ann Thorac Surg 1997;63: Van Son JAM, Falk V, Walther T, Smedts FM, Mohr FW. Low-grade intimal hyperplasia in internal mammary and right gastroepiploic arteries as bypass grafts. Ann Thorac Surg 1997;63: O Neil GS, Chester AH, Allen SP, et al. Endothelial function of human gastroepiploic artery. Implication for its use as a bypass graft. J Thorac Cardiovasc Surg 1991;102: Tavilla G, van Son JAM, Verhagen AF, Smedts F. Retrogastric versus antegastric routing and histology of the right gastroepiploic artery. Ann Thorac Surg 1992;53: Dignan RJ, Yeh T, Dyke CM, et al. Reactivity of gastroepiploic and internal mammary arteries. Relevance to coronary artery bypass grafting. J Thorac Cardiovasc Surg 1992;103: Hanet C, Semaan C, Khoury G, Dion R, Robert A. Differences in vasoreactivity between gastroepiploic artery grafts late after bypass surgery and grafted coronary arteries. Circulation 1994;90(Part 2): He G-W, Yang C-Q. Comparison among arterial grafts and coronary artery. An attempt at functional classification. J Thorac Cardiovasc Surg 1995;109: Malhotra R, Bedi HS, Bazaz S, Jain S, Trehan N. Morphometric analysis of the right gastroepiploic artery and the internal thoracic artery. Ann Thorac Surg 1996;61: Tedoriya T, Kawasuji M, Sakakibara N, Ueyama K, Watanabe Y. Pressure characteristics in arterial grafts for coronary bypass surgery. Cardiovasc Surg 1995;3: Dietl CA. Vascular reactivity of the gastroepiploic artery graft. J Thorac Cardiovasc Surg 1995;110: Tavilla G, Jackimovicz J, Berreklouw E. Intraoperative blood flow measurement of the right gastroepiploic artery using pulsed Doppler echocardiography. Ann Thorac Surg 1997;64: Albertini A, Lochegnies A, El Khoury G, et al. Use of the right gastroepiploic artery as a coronary artery bypass graft in 307 patients. Cardiovasc Surg 1998;6: Uchida N, Kawaue Y. Flow competition of the right gastroepiploic artery graft in coronary revascularization. Ann Thorac Surg 1996;62: Voutilainen S, Verkkala K, Järvinen A, Keto P. Angiographic 5-year follow-up study of right gastroepiploic artery grafts. Ann Thorac Surg 1996;62: He GW. Clinical physiology and related characteristics. In: He GW, ed. Arterial grafts for coronary artery bypass surgery. Singapore: Springer, 1999: Nishida H, Endo M, Koyanagi H, Koyanagi T, Nakamura K. Coronary artery bypass grafting with the right gastroepiploic artery and evaluation of flow with transcutaneous Doppler echocardiography. J Thorac Cardiovasc Surg 1994; 108: Piers LS, Soares MJ, McCormack LM, O Dea K. Is there evidence for an age-related reduction in metabolic rate? J Appl Physiol 1998;85: Olivetti G, Melissari M, Capasso JM, Anversa P. Cardiomyopathy of the aging human heart: myocyte loss and reactive cellular hypertrophy. Circ Res 1991;68: Lie JT, Hammond PI. Pathology of the senescent heart: autonomic observation on 237 autopsy studies of patients 90 to 105 years old. Mayo Clin Proc 1988;63:

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