Morphometric Study of the Right Gastroepiploic and Inferior Epigastric Arteries

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1 Morphometric Study of the Right Gastroepiploic and Inferior Epigastric Arteries Jacques A. M. van Son, MD, PhD, Frank M. Smedts, MD, PhD, Cheng-Qin Yang, MD, Marcel Mravunac, MD, Volkmar Falk, MD, Friedrich W. Mohr, MD, and Guo-Wei He, MD, PhD Herzzentrum, University of Leipzig, Leipzig, Germany; Canisius-Wilhelmina Hospital, Nijmegen, the Netherlands; and University of Hong Kong at Grantham Hospital, Hong Kong Background. Based on earlier observations that the thickness of the intima and structure of the media may have an impact on the long-term patency of arterial conduits and the lack of detailed histologic studies of the right gastroepiploic and inferior epigastric arteries, we subjected both vessels to morphometric analysis with emphasis on their suitability as conduits in myocardial revascularization. Methods. The right gastroepiploic and inferior epigastric arteries were harvested from 28 unselected individuals (mean age, 73.2 years) at autopsy, and the luminal diameter and the width of the intima and media were measured. Results. At all levels of measurement (origin, 10 cm, and 15 cm), the luminal diameter of the inferior epigastric artery was significantly smaller than that of the right gastroepiploic artery (p < 0.05). The right gastroepiploic artery demonstrated only mild intimal hyperplasia. In contrast, the inferior epigastric artery showed substantial intimal hyperplasia within the first 1-cm segment (mean, m versus m for the corresponding segment of the right gastroepiploic artery; p 0.01). Intimal hyperplasia was only mild in the remainder of the inferior epigastric artery. In both vessels, the media was muscular with rare dispersed elastic fibers. The mean thickness of the media ranged from m proximally to m distally for the right gastroepiploic artery, and from to m, respectively, for the inferior epigastric artery. Conclusions. In myocardial revascularization, use of the right gastroepiploic artery may generally be preferable to use of the inferior epigastric artery. This recommendation is based on the larger luminal diameter of the right gastroepiploic artery as compared with the inferior epigastric artery, the significantly greater intimal hyperplasia in the first segment of the inferior epigastric artery, and the limitation that the inferior epigastric artery can be used only as a free graft. The rate of development of intimal hyperplasia in the right gastroepiploic artery, if used as an in situ coronary artery bypass graft, may be slow, approximating that of the right gastroepiploic artery in its natural environment. (Ann Thorac Surg 1997;63:709 15) 1997 by The Society of Thoracic Surgeons Based on its superior long-term patency rates, the internal mammary artery (IMA) has emerged as the conduit of choice in myocardial revascularization [1 3]. Subsequent histologic and physiologic research has provided a detailed background regarding the morphology and function of this conduit [4 8]. Concomitant with the surge of interest in the IMA as a conduit in myocardial revascularization, other arterial conduits emerged, notably the right gastroepiploic artery (GEA) and the inferior epigastric artery (IEA), in the expectation of improving long-term patency rates as compared with venous conduits [9 14]. Based on the potential relation between structure of the media of the arterial conduit and the development of intimal hyperplasia, particularly if used as a free graft, and the lack of detailed histologic studies of the GEA and IEA, we conducted a morphometric study of both arteries. Accepted for publication Oct 15, Address reprint requests to Dr van Son, Herzzentrum, University of Leipzig, Russenstrasse 19, D-04289, Leipzig, Germany. Material and Methods Anatomy The right GEA is the larger of the two terminal branches of the gastroduodenal artery, the other being the superior pancreaticoduodenal artery. The GEA follows a course along the greater curvature of the stomach at a somewhat variable distance. It gives off a large ascending pyloric branch near its origin, and terminally it anastomoses with the left gastroepiploic branch of the splenic artery. It supplies several ascending branches to the stomach and descending branches to the greater omentum. The IEA arises from the medial aspect of the external iliac artery just proximal to the inguinal ligament. Accompanied in its course by two satellite veins. the IEA ascends obliquely and medially toward the umbilicus; after piercing the transversalis fascia, it enters the rectus sheath at the semilunar fold of Douglas. Direct arterial communications between the IEA and the superior epigastric artery may exist in the region of the umbilicus in approximately 40% of cases [15] by The Society of Thoracic Surgeons /97/$17.00 Published by Elsevier Science Inc PII S (96)

2 710 van SON ET AL Ann Thorac Surg GASTROEPIPLOIC AND INFERIOR EPIGASTRIC ARTERIES 1997;63: Fig 1. Gastroduodenal artery at origin of the right gastroepiploic artery. (A) Overview. (B) Detail showing moderate intimal hyperplasia and muscular character of the media. (Elastin-trichrome stain; original magnifications: A, 40; B, 100.) Arteries In this study, the GEA and the left (n 14) and right IEA (n 14) were obtained at autopsy from 28 unselected individuals (19 men, 9 women), between 55 and 91 years of age (mean age, 73.2 years), who had died of noncardiac diseases. The GEA was harvested from its origin at the gastroduodenal artery to its terminal anastomosis with the left gastroepiploic branch. The length of the GEA varied from 17 to 24 cm (mean standard deviation, 19 2 cm). The IEA was harvested from its origin at the external iliac artery to its terminal branch in the region of the umbilicus. The length of the IEA varied from 15 to 22 cm (mean standard deviation, 17 2 cm). Before fixation, the luminal diameters of the GEA and IEA were measured at the origin and at 10 and 15 cm using a semiautomatic image analyzing system (MOP Videoplan; Kontron, Munich, Germany). In all cases, the arteries were fixed in a flaccid state in 4% formaldehyde solution for 1 week. Each specimen was laminated in consecutive transverse sections at intervals of 1 cm, starting proximally at the origin of the GEA and IEA and ending at the distal segments of both arteries. Subsequently, these sections were embedded in paraffin and prepared in 4- m sections. Care was taken to ensure that these sections were not oblique and were not adjacent to branching points. All sections were stained with hematoxylin-eosin and elastin-trichrome techniques. The following measurements and observations were made: (1) The widths of the intima and media were measured at four random locations per section and a mean value was calculated; (2) the specific nature of the media (muscular versus elastic) was noted; and (3) the number of discontinuities in the circumferential internal elastic lamina was counted. Data are presented as mean standard deviation. Student s t test was used to assess differences in width of the intima and media and in the number of discontinuities in the internal elastic lamina between the proximal 50% and the distal 50% of the GEA and IEA. The differences in the mean luminal diameter and width of the intima and media between the GEA and IEA at corresponding distances were studied with analysis of variance. A p value less than 0.05 indicates a difference unlikely to be due to chance alone. Results Gastroepiploic Artery The gastroduodenal artery generally demonstrated mild to moderate intimal hyperplasia (Fig 1); however, its thickness in the immediate vicinity of the origin of the GEA was highly variable: m. The media of the gastroduodenal artery was muscular with rare dispersed elastic fibers (see Fig 1); its thickness was m. The mean luminal diameter of the GEA was mm at its origin, mm at 10 cm, and mm at 15 cm. The GEA generally showed mild intimal hyperplasia at its origin (intimal thickness, m), with a gradually decreasing degree of intimal hyperplasia along its course (distal intimal thickness, m) (p 0.003) (Figs 2, 3). The media of the GEA was muscular with rare dispersed elastic fibers (see Fig 2). The thickness of the media varied from m at the origin of the GEA to m distally (p ) (Fig 4). The number of discontinuities in the circumferential internal elastic lamina was rather constant, varying from at the origin to at 5 cm, and distally (p 0.79) (Fig 5). Inferior Epigastric Artery The external iliac artery showed moderate to severe intimal hyperplasia (Fig 6); the thickness of the intima in

3 Ann Thorac Surg van SON ET AL 1997;63: GASTROEPIPLOIC AND INFERIOR EPIGASTRIC ARTERIES 711 Fig 2. Right gastroepiploic artery. (A) Overview and (B) detail at origin from the gastroduodenal artery, (C) at 1 cm, (D) at 9 cm, and (E) at 18 cm. Note mild intimal hyperplasia (A) with focal moderate hyperplasia (B) at origin of the artery, decreasing intimal hyperplasia from proximal to distal, and muscular character of the media. (Elastin-trichrome stain; original magnifications: A, 40; B, 100; C E, 320.) the immediate vicinity of the origin of the IEA was m. The media of the external iliac artery was muscular with dispersed elastic fibers; its thickness was m. The mean luminal diameter of the IEA was mm at its origin, mm at 10 cm, and mm at 15 cm. At all three levels, the luminal diameter of the IEA was significantly smaller than that of the GEA (p 0.05). In contrast to the findings in the GEA, there was substantial intimal hyperplasia in the first 1-cm segment of the IEA (intimal thickness, m) (p 0.01); the width of the intima decreased to m at 1 cm and then gradually decreased to trivial values distally (p 0.01) (Figs 3, 7). The media of the IEA was muscular with rare dispersed elastic fibers (see Fig 7). The thickness of the media varied from m at 1cmto m distally (p ) (see Fig 4). The number of discontinuities in the circumferential internal elastic lamina was rather constant and varied from 82 25at3cmto35 11 distally (p 0.039) (see Fig 5). Comment Our recent work has classified arterial grafts according to the morphology of the media (elastic, elastomuscular, or muscular) and their reactivity toward vasoactive drugs [4, 5, 16]. It is still unclear, however, whether the histologic structure of the media of arterial conduits has an impact on their long-term patency. It is also unknown what relation exists between the contractility of an arterial conduit, which is usually proportional to the content of smooth muscle cells in its media, and its long-term patency. This study confirms the findings of earlier, albeit less detailed, histologic studies of the GEA, which reported only mild to moderate intimal thickening in this vessel in its natural state [17, 18]. In our recent histologic study of three GEAs obtained at autopsy that had served as in situ coronary artery bypass grafts to the right coronary artery for 19, 38, and 47 months [19], we demonstrated only mild intimal hyperplasia. Based on our results and those of

4 712 van SON ET AL Ann Thorac Surg GASTROEPIPLOIC AND INFERIOR EPIGASTRIC ARTERIES 1997;63: Fig 3. Thickness of intima in the right gastroepiploic artery (GEA) and the inferior epigastric artery (IEA). previous studies, we hypothesize that although the muscular character of the media of the GEA may increase its vulnerability to intimal thickening (as compared with the primarily elastic IMA), the development of intimal hyperplasia may be slow following a pattern that approximates that of the GEA in its natural environment if it is used as an in situ graft and thus is protected by retention in its usual physiologic environment. This hypothesis is corroborated by the clinical study of Grandjean and co-workers [10], in which they reported a patency rate of 84.5% at 10 months in 88 GEA conduits. With increasing surgical experience using the GEA, the same group Fig 4. Thickness of media in the right gastroepiploic artery (GEA) and the inferior epigastric artery (IEA).

5 Ann Thorac Surg van SON ET AL 1997;63: GASTROEPIPLOIC AND INFERIOR EPIGASTRIC ARTERIES 713 Fig 5. Number of discontinuities in the internal elastic lamina (IEL) in the right gastroepiploic artery (GEA) and the inferior epigastric artery (IEA). documented an early patency rate of 97% in their latest subset of patients, thus approximating or equaling the reported early patency rate of the IMA [1 3]. Similar patency rates of the GEA have been reported by Suma and colleagues [9] and Pym and associates [11]. Because of the great variability of intimal hyperplasia in the gastroduodenal artery as observed in this study, it may be advisable, particularly in older patients with diffuse coronary or systemic arterial disease, to perform preoperative angiography or intraoperative flow measurement of the GEA to rule out clinically relevant atherosclerotic lesions. In the present study, we observed that at its origin, the intima of the IEA is significantly thicker ( m) than that of the GEA in the corresponding segment (64 50 m) (p 0.01). Beyond 1 cm, there was only low-grade intimal hyperplasia in the IEA. This finding leads us to conclude that it may be better not to use the origin of the IEA because of the high likelihood of substantial intimal hyperplasia in this segment. Fig 6. External iliac artery at origin of the inferior epigastric artery. (A) Overview. (B) Detail showing moderate to severe intimal hyperplasia and muscular character of the media. (Elastin-trichrome stain; original magnifications: A, 32; B, 100.)

6 714 van SON ET AL Ann Thorac Surg GASTROEPIPLOIC AND INFERIOR EPIGASTRIC ARTERIES 1997;63: Fig 7. Inferior epigastric artery. (A) Overview and (B) detail at origin from the external iliac artery, (C) at 1 cm, (D) at 8 cm, and (E) at 16 cm. Note severe intimal hyperplasia in the first 1-cm segment, gradually decreasing degree of intimal hyperplasia beyond the first 1-cm segment, and muscular character of the media. (Elastin-trichrome stain; original magnifications: A, 32; B E, 320.) Buche and co-workers [14] reported a patency rate of 97% in 135 IEA conduits that were subjected to angiography within 2 weeks after myocardial revascularization. However, after restudy of 77 IEA conduits after an average period of 14.8 months, only 79% were widely patent. Dion and colleagues [3] reported a similar 80% patency rate for the free IMA (versus 96% for the in situ IMA graft) at 13 months postoperatively. However, Perrault and co-workers [13] performed immediate postoperative angiographic evaluation in 14 patients who had received an IEA graft mainly to the right coronary artery and reported that only eight grafts (57%) were patent. These data suggest that the size and morphologic characteristics of arterial grafts, if used as free grafts, may have a decisive impact on their patency rate. The difference in patency rates between the IEA and the free IMA graft may be related primarily to the smaller luminal diameter, reduced wall thickness, and muscular character of the media of the IEA as compared with the larger dimensions of the mainly elastic, and therefore more solid, IMA [4]. It is well known that creation of an anastomosis between the IEA and the aorta may be a technically awkward undertaking that probably should be performed only when favorable conditions are present, ie, a smooth aortic wall and a large-caliber IEA. To circumvent these problems, the proximal IEA may be anastomosed to the aorta on a hood of saphenous vein graft or to an IMA conduit. The latter technique, however, carries the risk of jeopardizing both arterial conduits and renders the entire left ventricular perfusion dependent on the sole IMA pedicle. With regard to long-term patency of the IEA, in addition to the fact that it can be used only as a free graft, morphologic and physiologic properties may be important. We predict that exposure of the muscular IEA to the high shear stresses of the central aortic circulation may lead to accelerated development of intimal hyperplasia. This prediction is based on the knowledge that the occurrence of discontinuities in the internal elastic lamina provokes early and progressive intimal hyperplasia caused by invasion of smooth muscle cells from the media through the fenestrated internal elastic lamina [20, 21]. In addition, as an indicator of suboptimal endothelial function in the IEA, probably secondary to intimal hyperplasia, we demonstrated a less potent nonreceptormediated endothelium-dependent relaxation in the IEA

7 Ann Thorac Surg van SON ET AL 1997;63: GASTROEPIPLOIC AND INFERIOR EPIGASTRIC ARTERIES 715 as compared with the IMA [22]. Other investigators have demonstrated that basal and stimulated release of nitric oxide in atherosclerotic human arteries is impaired [23, 24] and that the attenuation of the endotheliummediated vasodilation is selective [25]. Long-term clinical and histologic studies of the IEA will provide more insight into these factors and their influence on patency. We acknowledge the technical assistance of Wim van den Berg, CT, Canisius-Wilhelmina Hospital, Nijmegen, the Netherlands. References 1. Grondin CM, Campeau L, Lesperance J, Enjalbert M, Bourassa MG. Comparison of late changes in internal mammary artery and saphenous vein grafts in two consecutive series of patients 10 years after operation. Circulation 1984; 70(Suppl 1): Loop FD, Lytle BW, Cosgrove DM, et al. Influence of the internal mammary artery graft on 10-year survival and other cardiac events. N Engl J Med 1986;314: Dion R, Etienne PY, Verhelst R, et al. Bilateral mammary grafting. Clinical, functional and angiographic assessment in 400 consecutive patients. Eur J Cardiothorac Surg 1993;7: Van Son JAM, Smedts F, Vincent JG, van Lier HJJ, Kubat K. Comparative anatomic studies of various arterial conduits for myocardial revascularization. J Thorac Cardiovasc Surg 1990;99: Van Son JAM, Smedts F, de Wilde PCM, et al. Histological study of the internal mammary artery with emphasis on its suitability as a coronary artery bypass graft. Ann Thorac Surg 1993;55: Van Son JAM, Tavilla G, Noyez L. Detrimental sequelae on the wall of the internal mammary artery caused by hydrostatic dilation with diluted papaverine solution. J Thorac Cardiovasc Surg 1992;104: He GW. Contractility of the human internal mammary artery at the distal section increases toward the end. Emphasis on not using the end of the internal mammary artery for grafting. J Thorac Cardiovasc Surg 1993;106: He GW, Acuff TE, Yang CQ, Ryan WH, Mack MJ. Middle and proximal sections of the human internal mammary artery are not passive conduits. J Thorac Cardiovasc Surg 1994;108: 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: Grandjean JG, Boonstra PW, den Heyer P, Ebels T. Arterial revascularization with the right gastroepiploic artery and internal mammary arteries in 300 patients. J Thorac Cardiovasc Surg 1994;107: Pym J, Brown P, Pearson M, Parker J. Right gastroepiploicto-coronary artery bypass. The first decade of use. Circulation 1995;92(Suppl 2): Barner HB, Naunheim KS, Fiore AC, Fischer VW, Harris HH. Use of the inferior epigastric artery as a free graft for myocardial revascularization. Ann Thorac Surg 1991;52: Perrault LP, Carrier M, Hebert Y, Cartier R, Leclerc Y, Pelletier LC. Early experience with the inferior epigastric artery in coronary artery bypass grafting. J Thorac Cardiovasc Surg 1993;106: Buche M, Schroeder E, Gurné O, et al. Coronary artery bypass grafting with the inferior epigastric artery. Midterm clinical and angiographic results. J Thorac Cardiovasc Surg 1995;109: Millroy FJ, Anson BJ, McAfee DK. The rectus abdominis muscle and the epigastric arteries. Surg Gynecol Obstet 1960;110: He GW, Yang CQ. Comparison among arterial grafts and coronary artery. An attempt at functional classification. J Thorac Cardiovasc Surg 1995;109: Suma H, Takanashi R. Arteriosclerosis of the gastroepiploic and internal thoracic arteries. Ann Thorac Surg 1990;50: 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: 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: Ross R, Glomset JA. The pathogenesis of atherosclerosis (first of two parts). N Engl J Med 1976;295: Ross R, Glomset JA. The pathogenesis of atherosclerosis (second of two parts). N Engl J Med 1976;295: He GW, Acuff TE, Ryan WH, Yang CQ, Mack MJ. Functional comparison between the human inferior epigastric artery and internal mammary artery. Similarities and differences. J Thorac Cardiovasc Surg 1995;109: Chester AH, O Neill GS, Moncada S, Tadjkarimi S, Yacoub MH. Low basal and stimulated release of nitric oxide in atherosclerotic epicardial coronary arteries. Lancet 1990;336: Bossaler C, Habib GB, Yamamoto H, Williams C, Wells S, Henry PD. Impaired muscarinic endothelium-dependent relaxation and cyclic guanosine 5 -monophosphate formation in atherosclerotic human coronary artery and rabbit aorta. J Clin Invest 1987;79: Forstermann U, Mügge A, Alheid U, Haverich A, Frolich J. Selective attenuation of endothelium-mediated vasodilation in atherosclerotic human coronary artery. Circ Res 1988;62: