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Vascular anatomy of the gastrointestinal tract
Best Practice & Research Clinical Gastroenterology Vol. 15, No. 1, pp. 1±14, 2001
doi:10.1053/bega.2000.0152, available online at http://www.idealibrary.com on
1 Vascular anatomy of the gastrointestinal tract Karel Geboes*
MD, PhD
Professor in Pathology Department of Pathology, University Hospital, KULeuven, Minderbroedersstraat 12, 3000 Leuven, Belgium
Karen P. Geboes
MD, Resident
Department of Internal Medicine, University Hospital, KULeuven, Gasthuisberg, Herestraat 49, 3000 Leuven, Belgium
Geert Maleux
MD, Consultant
Department of Radiology, University Hospital, KULeuven, Gasthuisberg, Herestraat 49, 3000 Leuven, Belgium
The blood supply of the gastrointestinal system has intramural and extramural components. The intramural vascular distribution is generally well developed with plexuses in the dierent layers of the bowel wall and with specializations in the liver, small intestine and gastroesophageal junction, adapted to the function of these organs. The extramural arterial supply for the oesophagus is derived from the thoracic aorta or its major branches. Blood supply to the abdominal organs is provided by three major unpaired vessels arising from the abdominal aorta, namely the coeliac trunk and the superior and inferior mesenteric arteries. The branches of these vessels form anastomotic systems that provide a rich blood supply to the adjoining organs. In many areas the systems overlap while in other regions linkages are limited. Interrelations and weak points are of signi®cant clinical importance. As well as this, there is a great individual variability in the anatomy of the gastrointestinal vasculature. Key words: vascularization; oesophagus; stomach; liver; small and large intestine; coeliac trunk.
THE OESOPHAGUS Extramural pathways The extramural arterial supply of the human oesophagus is divided into three major segments, the cervical, thoracic and abdominal oesophagus, with numerous anastomoses.1 The pharyngo-oesophageal transition and cervical oesophagus are supplied by the lower thyroid artery, a branch of the thyrocervical trunk. An additional, individually variable supply is provided by small branches of other arteries such as the subclavian, common carotid, vertebral, superior thyroid and costocervical trunk. The right lower thyroid artery usually has more branches than the left, but the blood supply to both *All correspondence to K. Geboes, Department of Pathology. 1521±6918/01/01000114 $35.00/00
c 2001 Harcourt Publishers Ltd. *
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Figure 1. The arterial supply of the cricopharyngeus muscle (between arrows) is provided by branches of the laryngopharyngeal artery (1). The branches follow a sinusoidal pattern, parallel with the smooth muscle ®bres. They anastomose with similar branches of the opposite side (magni®cation 4) (with permission of Acta Gastroenterologica Belgica 1991; 53: 376±385).
sides of the oesophagus is of the same order. Two or three smaller branches of the lower thyroid artery supply the triangle of Laimer on the posterior wall of the cervical oesophagus where the muscle tissue is poorly developed. The upper edge of this V-shaped defect is formed by the cricopharyngeal muscle, which is supplied by small branches from the laryngopharyngeal artery, a branch of the lower thyroid. They originate following anastomosis between the laryngopharyngeal and the superior thyroid artery of the same side. They run parallel with the muscle ®bres of the cricopharyngeus and anastomose with analogous contralateral branches (Figure 1).2 The cervical oesophagus itself is supplied by the lower thyroid artery directly through ®nal branches and indirectly via rami oesophagi. The small ®nal branches enter the lateral wall of the oesophagus, and provide blood to the muscularis, the submucosa and mucosa. The thoracic oesophagus receives blood from branches of the aorta, the bronchial arteries and the right intercostal arteries. At the level of the bifurcation of the trachea, the main supply comes from branches of the bronchial arteries that descend on the ventral side of the oesophagus. Approximately 50% of all individuals have accessory oesophageal branches directly from the aorta, the internal mammary, the common carotid and upper intercostal arteries. Below the bifurcation of the trachea the blood supply originates from two oesophageal branches that arise directly from the right ventral side of the aorta. Both branches run to the dorsal side of the oesophagus where they split into a right and left branch. These in turn split into ascending and descending branches that anastomose between themselves, with the descending branches of the lower thyroid and with ascending branches of the left gastric and left lower phrenic artery.
Vascular anatomy of the GI tract 3
The abdominal oesophagus is supplied by oesophageal branches of the left gastric and left lower phrenic artery. They run alongside the right anterolateral and dorsal aspect of the oesophagus and anastomose with the lower two oesophageal branches from the thoracic aorta. An additional blood supply may be provided by branches of the aorta, the splenic artery, the coeliac trunk and an aberrant left hepatic artery.1 Intramural pathways The intramural arterial pattern is characterized by a well-developed subepithelial capillary network in the stromal papillae of the mucosa (intra-epithelial channels), supplied by a prominent submucosal arterial plexus. The plexus is composed of 9±12 longitudinally oriented arteries with lateral anastomoses and formed by penetrating branches arising from a minor extrinsic plexus in the adventitia.3,4 These branches pass at right angles through the muscle layer and give o, en route, branches to the muscle tissue and the myenteric plexus. Venous drainage Oesophageal veins are classi®ed into three groups: (i) intrinsic veins including subepithelial and submucosal veins that join the gastric veins below, and perforating veins which pierce the muscular wall to join the extrinsic veins; (ii) extrinsic veins formed by the union of groups of perforating veins that join the left gastric vein below and the systemic veins above; (iii) venae concomitantes that run longitudinally in the adventitia.5±7 The subepithelial or super®cial venous plexus drains the capillaries in the stromal papillae (Figure 2). It lies in the lamina propria, close to the epithelium and extends over the whole length of the oesophagus as a coarse polygonal meshwork.5 In the distal oesophagus, the veins follow a more longitudinal direction. In a segment extending over a distance of 1.5±3.5 cm from the oesophagogastric junction, they lie predominantly super®cially in the lamina propria.6±8 Numerous small veins perforate the muscularis mucosae to join larger veins of the submucosal plexus (deep intrinsic veins) lying midway between the muscularis mucosae and the circular muscle coat. The submucosal plexus consists of 10±15 longitudinal veins, evenly distributed around the circumference of the oesophagus and connected by numerous anastomoses. In its proximal part this plexus drains the longitudinally oriented veins from the ventral and dorsal pharyngo-oesophageal subepithelial plexus. At the distal end of the oesophagus, the longitudinal submucosal veins increase in number but decrease in diameter. At the cardia, they become tortuous and aggregate in the longitudinal folds of the mucosa before joining the submucosal veins of the stomach. Perforating veins arise from the longitudinal submucosal plexus and pass through the muscle layer, which they also drain, at regular intervals. The greater extrinsic peri-oesophageal veins include two larger and several smaller veins. The larger veins run longitudinally on the outer surface in close proximity to the vagus nerves and connect the left gastric vein to the azygos or hemiazygos veins either directly or via the posterior bronchial veins. Other veins are the cervical perioesophageal veins draining into the inferior thyroid, vertebral and deep cervical veins, small oesophageal veins at the cardia joining the superior and inferior phrenic veins and small abdominal oesophageal veins draining into the left gastric vein but also the vena phrenica inferior, gastroepiploica and splenica.5
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Figure 2. Intramural venous drainage of the oesophagus. The capillaries in the stromal papillae (1) are drained by a subepithelial plexus (2), which itself is drained by the super®cial venus plexus in the mucosa (3) (magni®cation 52) (with permission of Acta Gastroenterologica Belgica 1991; 53: 376±385).
THE ABDOMINAL ORGANS Intramural pathways The stomach The gastric blood supply is derived from the common hepatic, left gastric and splenic arteries arising from the coeliac trunk. Branches of the hepatic artery known as the right gastric artery and the right gastroepiploic artery, supply the lesser and distal greater curve, respectively. The proximal greater curve is supplied by the left gastroepiploic artery and by short gastric arteries from the splenic artery. The vessels form two extrinsic arcading anastomotic loops. The superior loop between the right and left gastric artery lies in the lesser omentum close to the lesser curve. The inferior loop between the right and left gastroepiploic lies in the greater omentum close to the greater curve. The loops give o a series of short branches to the anterior and posterior walls. The fundus and left margin of the greater curve are supplied by ®ve short gastric arteries derived from the splenic artery. The branches from the loops form a subserosal plexus.9±11 Perforating branches originating from this plexus, pass through the external muscle layers of the gastric wall to reach a richly anastomotic submucosal arterial plexus. Small side branches are given o to the external muscle layers and to Auerbach's plexus en route, but the majority of arterioles to the external muscle come from the submucosal plexus. The submucosal arterial network extends between the greater and lesser curves and provides anastomoses between the vessels derived from the lesser and those from the greater curves. The mucosa is supplied by small branches from the submucosal plexus, which pass perpendicularly through the
Vascular anatomy of the GI tract 5
OESOPHAGUS SQUAMOUS EPITHELIUM
STOMACH CN
Intraepithelial channels
MUSC. MUCOSAE SUBMUCOSA
MUSCULARIS PROPRIA SA
ADVENTITIA
SMALL INTESTINE
COLON CN
VC MUCOSA VA MUSC. MUCOSAE SUBMUCOSA
CC
SAP
CA
SAP
MUSCULARIS PROPRIA
VR VR
MA MA
Figure 3. Intramural arterial distribution in the oesophagus, stomach, small intestine and colon. Abbreviations are: CA, cryptal arteriole; CC, capillaries; CN, capillary network; MA, marginal artery; SA, supplying artery; SAP, submucosal arterial plexus; VA, villous arteriole; VC, villous capillaries; VR, vasa recta.
muscularis mucosae. In the lamina propria the arterioles branch into capillaries, which run towards the lumenal surface between the gastric glands. There are frequent cross anastomoses between adjacent capillaries. Just underneath the surface epithelium, the capillaries form a polygonal network around the necks of the gastric pits (Figure 3).12±16 Mucosal venules drain into the submucosal venous plexus, which is continuous with a similar plexus in the oesophagus and duodenum. In the gastric cardia the submucosal venous plexus is composed of a series of parallel veins oriented towards the oesophagogastric junction. Drainage of the muscle layers occurs to the submucosal venous plexus and partly to perforating veins, which pass to subserosal veins. The latter drain to arcading veins in the omenta and towards the portal system.
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The small intestine The duodenum is supplied chie¯y by the pancreaticoduodenal artery o the coeliac trunk. The jejunum and the ileum are supplied by a dozen branches o the superior mesenteric artery. These branches divide and anastomose several times in the mesentery, forming arcades. The last of these forms a marginal artery along the small intestine. The marginal artery is de®ned as the artery closest to, and parallel with, the wall of the intestine. From the marginal artery, blood reaches the intestine by way of short, straight branches or `vasa recta'. In the upper jejunum there are only one or two arcades and the vasa recta are 3±5 cm long. Arcades increase in number up to ®ve towards the distal ileum and the vasa recta become short. The vasa recta penetrate the external muscle layers of the bowel wall to reach a profusely anastomotic submucosal arterial plexus from which arterioles originate for the mucosa, submucosa and muscular layers. The submucosal plexus gives o two types of mucosal branches: long or villous arterioles and short or cryptal ones. Arterioles to the villi pass without branching into the lamina propria. At the tip of the villus the arteriole splays into a network of capillaries that subsequently course down along the sides of the villus in a fountain-like pattern. The crypts receive their arterial supply adjacent to the muscularis mucosae. The lymphoid tissue of the small intestine is supplied by the submucosal plexus through interfollicular arteries between the lymphoid follicles and through follicular arterioles originating from the interfollicular arteries. In Peyer's patches, some of the follicular arterioles directly supply a domelike capillary network beneath the epithelium overlying the follicles. Venous drainage of each of the small intestinal capillary beds passes to the submucosal venous plexus, which anastomoses both longitudinally and circumferentially in the bowel wall. This plexus is drained by short veins, which penetrate the external muscle layers, chie¯y along the mesenteric margin and then pass to branches of the superior mesenteric vein in the mesentery. The superior mesenteric vein receives venous drainage of the distal duodenum, the jejunum, ileum, appendix and caecum, the ascending and transverse colon and a right gastro-epiploic vein draining the stomach, before joining the splenic vein to form the hepatic portal vein.12,14,17 The large intestine Ascending and transverse colon are supplied by three branches of the superior mesenteric artery (ileocolic and right and middle colic arteries), whereas the splenic ¯exure, descending colon and sigmoid are nourished by branches of the inferior mesenteric artery (left colic and sigmoid arteries). These vessels form arcades that are less numerous and less complex than those in the small intestine. Within 2 cm of the colon wall, a single large anastomotic marginal artery is formed. This marginal artery runs retroperitoneally, extending from the ileocaecal junction down to and into the sigmoid mesocolon close to its attachment to the colon wall, thus forming an anastomotic channel between ileocolic, right, middle and left colic and sigmoid arteries. The rectum has a richly anastomosing arterial system derived from the inferior mesenteric and internal iliac arteries. Through the superior rectal artery it forms an anastomosis with the marginal artery of the colon. Short vasa recta pass from the marginal artery to the colon wall, with few or no anastomoses en route. Upon reaching the wall, they divide to form subserosal branches that pass circumferentially around the bowel wall and other branches that form a subserosal anastomosing plexus. The subserosal plexus gives o branches that traverse the external muscle coat to
Vascular anatomy of the GI tract 7
reach the submucosal arterial plexus. There is extensive anastomosis in the submucosa both longitudinally and circumferentially. Arteriolar branches from the submucosal plexus penetrate the muscularis mucosae and then break up in a chain of capillaries. These capillaries ascend along the glands and reach the surface of the mucosa where they form a honeycomb pattern around the openings of the glands, just beneath the surface epithelium. The muscularis contains capillaries derived from both the subserosal and submucosal plexuses and is perforated by larger arteries coming from the serosa and subserosa. The venous drainage largely parallels the arterial supply.12,18 The pancreas The arterial supply consists of variable branches from the coeliac trunk and the superior mesenteric artery. Arterial arcades are formed between the major supply arteries, and there are numerous anastomoses within the substance of the pancreas. Within the pancreas the arterial branches form an interlobular plexus in the connective tissue of the interlobular septa. From these plexuses single intralobular arteries pass into each lobule where they form glomerula-like tufts supplying individual islets of Langerhans and then continue to adjacent acini. Thus, a portal type of system is formed where the exocrine pancreas receives blood rich in islet-cell hormones. The veins in the pancreas correspond in general to the arterial pattern. They drain into the portal venous system behind the neck of the pancreas.19 The liver The portal vein is formed by the union of the superior mesenteric and splenic veins, and delivers blood to the liver through the hilum. This vein then progressively divides into smaller terminal branches that supply about 70% of oxygen to the liver parenchyma. The arterial blood is supplied by the hepatic artery. The right lobe of the liver is supplied by the right hepatic artery. The left lobe draws its blood from several sources. The lateral segment derives its supply from the left hepatic artery. The quadrate lobe (medial segment of the left lobe) obtains its arterial blood predominantly from the middle hepatic artery. Small branches from the left hepatic artery can augment this. Blood for the caudate lobe usually comes from the right hepatic artery, but in some instances, left or even middle hepatic arteries contribute. Once the hepatic arteries have penetrated the hepatic parenchyma, they arborize in the portal tracts alongside the portal vein and form two plexuses before delivering their blood into the liver sinusoids. One plexus is around small portal vein radicles and the other around small bile ducts. From the terminal portal veins and hepatic arterioles sprout small side branches that feed directly into the hepatic sinusoids where blood from both sources mixes in the intercommunicating complex of sinusoids. These are unique vessels lined by fenestrated endothelial cells without tight junctions and phagocytic Kuper cells. Sinusoids drain slowly into terminal hepatic veins. These join up to form the main hepatic veins that empty into the inferior vena cava just below its junction with the right atrium.20 The extramural splanchnic circulation The coeliac trunk The coeliac trunk is a short (2 cm) large (5±8 mm) artery that arises from the front of the aorta, usually at the twelfth thoracic±®rst lumbar vertebral level between the
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Figure 4. Selective angiogram of a normal coeliac trunk (a) showing the common hepatic artery (b), the right (c) and left (d) hepatic arteries, the left gastric artery (e), the splenic artery (f) and the gastroduodenal artery (g).
crura of the diaphragm. It passes horizontally forward above the upper margin of the pancreas. It divides almost immediately into three branches: the common hepatic, splenic and left gastric arteries (Figure 4). There are however many variations of the typical origin. The most striking of these is a common origin of the coeliac trunk and the superior mesenteric artery in a coeliacomesenteric trunk (in approximately 2% of cases). In this situation a single artery is the sole source of vascularization of the supramesocolic organs. Collateral ¯ow is only possible from the inferior mesenteric, phrenic, oesophageal and retroperitoneal arteries.9
The hepatic artery The common hepatic artery arises on the right side of the coeliac trunk and runs superiorly along the upper border of the head of the pancreas forward and to the right, giving o branches to the stomach, duodenum and pancreas. Where the gastroduodenal artery branches o, it becomes the hepatic artery proper. This artery enters the porta hepatis to the right with the hepatic duct lying to its right and the portal vein behind and divides into the right, left and middle hepatic artery. In approximately 18% of patients the hepatic artery does not originate from the coeliac trunk but emerges partially or entirely from the superior mesenteric artery. The hepatic artery is termed `replaced' when there is no other artery from the coeliac trunk supplying the same liver lobe. It is termed `accessory' when it occurs in addition to one from the coeliac trunk.
Vascular anatomy of the GI tract 9
The cystic artery typically arises to the right of the common hepatic duct from the right hepatic artery but has another origin in about 20% of cases. Reaching the gallbladder, it divides into a super®cial and a deep branch, the former being distributive to the peritoneal surface and the latter to the non-peritoneal surface of the gallbladder. Variations in the pattern of the hepatic arterial blood supply are extremely frequent. The right gastric artery is a small branch that arises from the common hepatic or left hepatic artery in about equal proportions (40%) and less frequently from the gastroduodenal artery (8%) or the middle or right hepatic artery (5%). It descends to the pylorus along the lesser curvature of the stomach where it usually anastomoses with the left gastric artery. The right gastric artery frequently gives rise to the supraduodenal artery (of Wilkie). The gastroduodenal artery usually arises from the common hepatic artery (75%) but may arise from the left or right hepatic artery or superior mesenteric artery. It descends behind the ®rst part of the duodenum anterior to the pancreas and courses to the left where it divides into the right gastroepiploic and the anterior superior pancreaticoduodenal arteries. In the majority of instances (90%) it gives rise to the `retroduodenal artery', which provides the blood supply to the common bile duct. Behind the intrapancreatic portion of the common bile duct, this artery anastomoses with the posterior inferior pancreaticoduodenal artery to form the pancreaticoduodenal arcade supplying the posterior surface of the entire duodenum and the head of the pancreas. The anterior pancreaticoduodenal arcade is formed behind the head of the pancreas by the anastomosis between the anterior superior pancreaticoduodenal artery and the anterior inferior pancreaticoduodenal artery, which arises from the superior mesenteric artery. The right gastroepiploic artery is the ®nal continuation of the gastroduodenal artery. After supplying one or more branches to the pylorus, it passes to the left along the greater curvature of the stomach. Ascending branches supply the greater curvature of the stomach and anastomose with descending branches of the right and left gastric arteries. The right gastroepiploic artery is also involved in the posterior omental arcade (Barkow) formed by the right epiploic (arising from the right gastroepiploic) and left epiploic (arising from the left gastroepiploic, a branch of the splenic artery) arteries. Branches from the omental arcade anastomose with branches from the middle and left colic, inferior pancreaticoduodenal and transverse pancreatic arteries. The left gastric artery The left gastric artery courses upwards to the left toward the gastric cardia, where it turns sharply downward and, following the lesser curvature, descends to the right toward the pylorus. It supplies part of the stomach and the inferior oesophagus. The anastomosis with the right gastric artery may be absent. In 25% of cases the left gastric artery gives rise to an aberrant left hepatic artery. The splenic artery The splenic artery arises from the coeliac artery, takes a short loop to the right, and then courses to the left along the cephalic border of the pancreas to supply the spleen. It gives o branches to the pancreas and stomach. The ®rst large pancreatic branch is the dorsal pancreatic artery, which in approximately 40% of the cases arises from the ®rst portion of the splenic artery but in 60% from other sources such as the right
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hepatic, superior mesenteric or coeliac arteries. The dorsal pancreatic artery descends and supplies branches to the posterior surface of the pancreas and gives o the transverse pancreatic artery, which courses to the left to supply the body and tail. The dorsal pancreatic artery gives o two branches to the right. One is joining the anterior superior pancreaticoduodenal, the gastroduodenal, or the right gastroepiploic artery and the other supplies the uncinate process. Often, a fourth branch of the dorsal pancreatic artery descends below the inferior border of the pancreas to communicate with the superior mesenteric artery. Occasionally, this branch gives rise to the middle colic artery (artery of Riolan). The arteria pancreatica magna arises from the second segment of the splenic artery and joins the transverse pancreatic artery. The caudal pancreatic arteries, which are often multiple, arise from the third and fourth segments of the splenic artery. They enter the tail of the pancreas and join branches of both, the arteria pancreatica magna and the transverse pancreatic artery. The latter may arise either from the superior mesenteric artery or the gastroduodenal artery. The left gastroepiploic artery arises from the splenic artery prior to its terminal divisions or from a terminal division itself. It courses downward to the right in the great omentum along the greater curvature of the stomach. It gives o the left epiploic artery that anastomoses with the right epiploic artery, a branch of the right gastroepiploic artery, to form the arcus epiploicus magnus of Barkow, in the great omentum below the colon. Short gastric arteries originate from the distal splenic artery and supply the fundus and cardia of the stomach. Superior mesenteric artery The superior mesenteric artery originates from the aorta at the level of the ®rst lumbar vertebra, behind the body of the pancreas. It emerges from under the lower border of the pancreas, passes forward anteriorly over the upper border of the third portion of the duodenum and descends anteriorly into the mesentery. Usually, the middle colic artery arises from the superior mesenteric artery just before it enters the mesentery. The middle colic artery can arise as a separate branch or be derived from a common right colic-middle colic trunk (53% of the cases). Occasionally, it arises directly from the coeliac artery. When the middle colic artery has a large branch running parallel and posterior to it in the transverse mesocolon, this branch is often described as the arc of Riolan. The right colic artery can arise directly (38%) from the superior mesenteric artery. The middle and right colic arteries supply the right half of the transverse colon and the ascending colon. Within the mesentery, the superior mesenteric artery courses to the right iliac fossa, curving to the left to end in the ileocolic artery by forming an anastomosis. Major side branches of the superior mesenteric artery originating usually on the right side are the inferior pancreaticoduodenal arteries supplying the lower part of the duodenum. In approximately 60% of cases there are two inferior pancreaticoduodenal arteries, but in 40% there is only one common inferior pancreaticoduodenal artery. These arteries connect with the superior pancreaticoduodenal arteries. The inferior pancreaticoduodenal artery can also arise from, or in common with, the ®rst jejunal artery. To the left, 4±6 jejunal arteries, and 9±13 intestinal branches that supply the ileum can be identi®ed. These are often called `intestinal arteries'. They divide into two branches, forming a ®rst order arcading anastomosis with the neighbouring branches. Subsequent anastomoses form second- to fourth-order arcades. Branches of these arcades ®nally form the marginal artery. The marginal artery may thus be composed of arteries that range
Vascular anatomy of the GI tract 11
Figure 5. Selective superior mesenteric angiogram showing the main branches to small bowel and right colon: (a) superior mesenteric artery, (b) jejunal arteries, (c) ileal arteries, (d) ileocolic artery, (e) right colic artery, (f) middle colic artery.
from third- or fourth-order arcades to the parent colic artery itself. The middle colic artery is often the marginal artery for the major portion of its distribution. Fine branches originating from the marginal artery reach the bowel wall as `vasa recta'. The vasa recta of the small intestine are shorter, closer together and less straight in appearance than the large bowel vasa recta. The terminal branch of the superior mesenteric artery is the ileocolic artery. It distributes branches to the terminal ileum, the caecum and the lower third or half of the ascending colon (Figure 5). In its distal distribution the ileal and colic branches of the ileocolic artery often form an `ileocolic loop'. The anterior and posterior caecal arteries and the appendicular artery arise separately from this loop. Inferior mesenteric artery The inferior mesenteric artery arises from the aorta anteriorly at the level of the third lumbar vertebra and descends to the left (Figure 6). Major side branches are the left colic artery and the sigmoidal arteries. The descending branch of the inferior mesenteric artery becomes the superior rectal artery. The left colic artery is usually an ascending branch from the inferior mesenteric artery. This branch bifurcates at the splenic ¯exure, its right branch joining the middle colic artery from the superior
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Figure 6. Selective angiogram of the inferior mesenteric artery showing the main branches of the left colon: (a) inferior mesenteric artery, (b) ascending branch, (c) marginal artery, (d) vasa recta, (e) descending branch and (f) sigmoid artery.
mesenteric artery and its left branch joining the marginal artery. Sigmoidal arteries can originate from the ascending branch in common with the left colic, or arise from a descending branch of the inferior mesenteric artery. A few sigmoidal arteries may arise from a middle branch. The number of sigmoid arteries varies from one to ®ve. The superior rectal artery divides into two branches of unequal size at the level of the second or third sacral vertebra, commonly at the bottom of the pouch of Douglas. The larger right branch divides into several branches that descend on the posterior and lateral surface of the rectal ampulla. The smaller, left branch deviates to the left and supplies the lateral and anterior surface. In contrast to the small and large intestinal arteries, the branches of the rectal arteries do not form arcades but enter the gut wall directly and independently. The branches of the superior rectal artery further anastomose with the middle and inferior rectal arteries originating, respectively, from the internal iliac and pudendal arteries.9±11 Venous drainage The venous blood from the gastrointestinal organs and spleen is drained by the hepatic portal circulation through the liver before it returns to the heart. The hepatic portal vein is formed by the union of the superior mesenteric and splenic veins. The superior
Vascular anatomy of the GI tract 13
mesenteric vein drains blood from the pancreas, the stomach, the small intestine and portions of the large intestine through the pancreaticoduodenal, right gastroepiploic, jejunal, ileal, ileocolic, right and middle colic veins. The splenic vein drains blood from the stomach, pancreas and portions of the large intestine through the short gastric, left gastroepiploic, pancreatic and inferior mesenteric veins. The inferior mesenteric vein, which passes into the splenic vein, drains portions of the large intestine through the superior rectal, sigmoidal and left colic veins. The right and left gastric veins, which open directly into the hepatic portal vein, drain large portions of the stomach. The cystic vein, which drains the gallbladder, also opens into the hepatic portal vein. COLLATERAL BLOOD SUPPLY The various pathways can be subdivided into six categories: channels between the coeliac trunk and the superior mesenteric artery; between the coeliac trunk and the aorta; between the dierent coeliac branches; between superior mesenteric branches; connections between the superior and inferior mesenteric artery; routes between the inferior mesenteric artery and parietal branches of the aorta. SUMMARY The blood supply of the gastrointestinal system has been studied extensively. Both the intramural and extramural vascular supply and their variants are well known. The arterial blood supply to the oesophagus is complex. The upper third is supplied by the inferior thyroid arteries, the mid third by intercostal and bronchial arteries and branches from the aorta and the lower third by the left gastric and phrenic arteries. There are anastomoses among the various components. The arterial supply of the stomach is provided by branches of the coeliac trunk. The small intestine is supplied primarily from the superior mesenteric artery and the colon is provided by branches from the superior and inferior mesenteric arteries. There are many collaterals between the dierent systems. The venous return largely parallels the arterial supply. REFERENCES
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*
1. Franssen G & Valembois P. Anatomy and embryology. In Vantrappen G & Hellemans J (eds) Disease of the esophagus, pp 1±16. Berlin: Springer Verlag, 1974. 2. Ramaekers D, Mebis J, Geboes K & Desmet V. De vascularisatie van de faryngo-oesofageale transitiezone. Acta Gastroenterologica Belgica 1991; 53: 376±385. 3. Potter SE & Holyoke EA. Observations on the intrinsic blood supply of the esophagus. Archives of Surgery 1950; 61: 944±948. 4. Shapiro AL & Robillard GL. The esophageal arteries: their con®gurational anatomy and variations in relation to surgery. Annals of Surgery 1950; 131: 171±185. 5. Butler H. The veins of the oesophagus. Thorax 1951; 6: 276±296. 6. Kitano S, Terblanche J, Kahn D & Bornman PC. Venous anatomy of the lower oesophagus in portal hypertension: practical implications. British Journal of Surgery 1986; 73: 525±531. 7. Spence RAJ. The venous anatomy of the lower oesophagus in normal subjects and in patients with varices: an image analysis study. British Journal of Surgery 1984; 71: 739±744. 8. Noda T. Angioarchitectural study of esophageal varices with special reference to variceal rupture. Virchows Arch iv A. Pathological Anatomy and Histology 1984; 404: 381±392. 9. Kornblith PL, Boley SJ & Whitehouse BS. Anatomy of the splanchnic circulation. Surgical Clinics of North America 1992; 72: 1±30.
14 K. Geboes et al 10. Wenz W (ed.). RoÈntgenanatomie der AbdominalgefaÈsse. In: Abdominale angiographie, pp 3±7. Berlin: Springer Verlag, 1972. *11. Putz R & Pabst R (eds) Sobotta atlas of human anatomy, pp 130±259. Munich: Urban & Schwarzenberg, 1997. *12. Gannon B. The vasculature and lymphatic drainage. In Whitehead R (ed.) Gastrointestinal and oesophageal pathology, 2nd edn. pp 129±199. Edinburgh: Churchill Livingstone, 1995. *13. Gannon B, Browning S, O'Brien P & Rogers P. Mucosal microvascular architecture of the fundus and body of the human stomach. Gastroenterology 1984; 86: 866±875. 14. Piasecki C. Blood supply to the human gastroduodenal mucosa with special reference to the ulcer bearing areas. Journal of Anatomy 1974; 118: 295±354. *15. Ohtsuka A, Ohtani O & Murakami T. Microvascularization of the alimentary canal as studied by scanning electron microscopy of corrosion casts. In Motta PM & Fujita H (eds) Ultastructure of the digestive tract, pp 201±212. Boston: Martinus Nijho Publishers, 1988. *16. Matsuura T & Yamamoto T. An electron microscope study of arteriolar branching sites in the normal gastric submucosa of rats and in experimental ulcer. Virchows Archiv A Pathological Anatomy and Histology 1988; 413: 123±131. 17. Gannon BJ, Rogers PAW & O'Brien PAW. Two capillary plexuses in human intestinal villi. Micron 1980; 11: 447±448. 18. Wolfram-Gabrel R, Maillot CL & Koritke JG. SysteÂmatisation de l'angioarchitecture du colon chez l'homme adulte. Acta Anatomica 1986; 125: 65±72. 19. Harris PF. Anatomy. In Howat HT & Sarles H (eds) The exocrine pancreas, pp 15±30. London: W.B. Saunders Company, 1979. *20. MacSween RNM & Scothorne RJ. Developmental anatomy and normal structure. In MacSween RNM, Anthony PP, Scheuer PJ, Burt A & Portmann BC (eds) Pathology of the liver, 3rd edn. pp 1±50. Edinburgh: Churchill Livingstone, 1994.
doi:10.1053/bega.2000.0152, available online at http://www.idealibrary.com on
1 Vascular anatomy of the gastrointestinal tract Karel Geboes*
MD, PhD
Professor in Pathology Department of Pathology, University Hospital, KULeuven, Minderbroedersstraat 12, 3000 Leuven, Belgium
Karen P. Geboes
MD, Resident
Department of Internal Medicine, University Hospital, KULeuven, Gasthuisberg, Herestraat 49, 3000 Leuven, Belgium
Geert Maleux
MD, Consultant
Department of Radiology, University Hospital, KULeuven, Gasthuisberg, Herestraat 49, 3000 Leuven, Belgium
The blood supply of the gastrointestinal system has intramural and extramural components. The intramural vascular distribution is generally well developed with plexuses in the dierent layers of the bowel wall and with specializations in the liver, small intestine and gastroesophageal junction, adapted to the function of these organs. The extramural arterial supply for the oesophagus is derived from the thoracic aorta or its major branches. Blood supply to the abdominal organs is provided by three major unpaired vessels arising from the abdominal aorta, namely the coeliac trunk and the superior and inferior mesenteric arteries. The branches of these vessels form anastomotic systems that provide a rich blood supply to the adjoining organs. In many areas the systems overlap while in other regions linkages are limited. Interrelations and weak points are of signi®cant clinical importance. As well as this, there is a great individual variability in the anatomy of the gastrointestinal vasculature. Key words: vascularization; oesophagus; stomach; liver; small and large intestine; coeliac trunk.
THE OESOPHAGUS Extramural pathways The extramural arterial supply of the human oesophagus is divided into three major segments, the cervical, thoracic and abdominal oesophagus, with numerous anastomoses.1 The pharyngo-oesophageal transition and cervical oesophagus are supplied by the lower thyroid artery, a branch of the thyrocervical trunk. An additional, individually variable supply is provided by small branches of other arteries such as the subclavian, common carotid, vertebral, superior thyroid and costocervical trunk. The right lower thyroid artery usually has more branches than the left, but the blood supply to both *All correspondence to K. Geboes, Department of Pathology. 1521±6918/01/01000114 $35.00/00
c 2001 Harcourt Publishers Ltd. *
2 K. Geboes et al
Figure 1. The arterial supply of the cricopharyngeus muscle (between arrows) is provided by branches of the laryngopharyngeal artery (1). The branches follow a sinusoidal pattern, parallel with the smooth muscle ®bres. They anastomose with similar branches of the opposite side (magni®cation 4) (with permission of Acta Gastroenterologica Belgica 1991; 53: 376±385).
sides of the oesophagus is of the same order. Two or three smaller branches of the lower thyroid artery supply the triangle of Laimer on the posterior wall of the cervical oesophagus where the muscle tissue is poorly developed. The upper edge of this V-shaped defect is formed by the cricopharyngeal muscle, which is supplied by small branches from the laryngopharyngeal artery, a branch of the lower thyroid. They originate following anastomosis between the laryngopharyngeal and the superior thyroid artery of the same side. They run parallel with the muscle ®bres of the cricopharyngeus and anastomose with analogous contralateral branches (Figure 1).2 The cervical oesophagus itself is supplied by the lower thyroid artery directly through ®nal branches and indirectly via rami oesophagi. The small ®nal branches enter the lateral wall of the oesophagus, and provide blood to the muscularis, the submucosa and mucosa. The thoracic oesophagus receives blood from branches of the aorta, the bronchial arteries and the right intercostal arteries. At the level of the bifurcation of the trachea, the main supply comes from branches of the bronchial arteries that descend on the ventral side of the oesophagus. Approximately 50% of all individuals have accessory oesophageal branches directly from the aorta, the internal mammary, the common carotid and upper intercostal arteries. Below the bifurcation of the trachea the blood supply originates from two oesophageal branches that arise directly from the right ventral side of the aorta. Both branches run to the dorsal side of the oesophagus where they split into a right and left branch. These in turn split into ascending and descending branches that anastomose between themselves, with the descending branches of the lower thyroid and with ascending branches of the left gastric and left lower phrenic artery.
Vascular anatomy of the GI tract 3
The abdominal oesophagus is supplied by oesophageal branches of the left gastric and left lower phrenic artery. They run alongside the right anterolateral and dorsal aspect of the oesophagus and anastomose with the lower two oesophageal branches from the thoracic aorta. An additional blood supply may be provided by branches of the aorta, the splenic artery, the coeliac trunk and an aberrant left hepatic artery.1 Intramural pathways The intramural arterial pattern is characterized by a well-developed subepithelial capillary network in the stromal papillae of the mucosa (intra-epithelial channels), supplied by a prominent submucosal arterial plexus. The plexus is composed of 9±12 longitudinally oriented arteries with lateral anastomoses and formed by penetrating branches arising from a minor extrinsic plexus in the adventitia.3,4 These branches pass at right angles through the muscle layer and give o, en route, branches to the muscle tissue and the myenteric plexus. Venous drainage Oesophageal veins are classi®ed into three groups: (i) intrinsic veins including subepithelial and submucosal veins that join the gastric veins below, and perforating veins which pierce the muscular wall to join the extrinsic veins; (ii) extrinsic veins formed by the union of groups of perforating veins that join the left gastric vein below and the systemic veins above; (iii) venae concomitantes that run longitudinally in the adventitia.5±7 The subepithelial or super®cial venous plexus drains the capillaries in the stromal papillae (Figure 2). It lies in the lamina propria, close to the epithelium and extends over the whole length of the oesophagus as a coarse polygonal meshwork.5 In the distal oesophagus, the veins follow a more longitudinal direction. In a segment extending over a distance of 1.5±3.5 cm from the oesophagogastric junction, they lie predominantly super®cially in the lamina propria.6±8 Numerous small veins perforate the muscularis mucosae to join larger veins of the submucosal plexus (deep intrinsic veins) lying midway between the muscularis mucosae and the circular muscle coat. The submucosal plexus consists of 10±15 longitudinal veins, evenly distributed around the circumference of the oesophagus and connected by numerous anastomoses. In its proximal part this plexus drains the longitudinally oriented veins from the ventral and dorsal pharyngo-oesophageal subepithelial plexus. At the distal end of the oesophagus, the longitudinal submucosal veins increase in number but decrease in diameter. At the cardia, they become tortuous and aggregate in the longitudinal folds of the mucosa before joining the submucosal veins of the stomach. Perforating veins arise from the longitudinal submucosal plexus and pass through the muscle layer, which they also drain, at regular intervals. The greater extrinsic peri-oesophageal veins include two larger and several smaller veins. The larger veins run longitudinally on the outer surface in close proximity to the vagus nerves and connect the left gastric vein to the azygos or hemiazygos veins either directly or via the posterior bronchial veins. Other veins are the cervical perioesophageal veins draining into the inferior thyroid, vertebral and deep cervical veins, small oesophageal veins at the cardia joining the superior and inferior phrenic veins and small abdominal oesophageal veins draining into the left gastric vein but also the vena phrenica inferior, gastroepiploica and splenica.5
4 K. Geboes et al
Figure 2. Intramural venous drainage of the oesophagus. The capillaries in the stromal papillae (1) are drained by a subepithelial plexus (2), which itself is drained by the super®cial venus plexus in the mucosa (3) (magni®cation 52) (with permission of Acta Gastroenterologica Belgica 1991; 53: 376±385).
THE ABDOMINAL ORGANS Intramural pathways The stomach The gastric blood supply is derived from the common hepatic, left gastric and splenic arteries arising from the coeliac trunk. Branches of the hepatic artery known as the right gastric artery and the right gastroepiploic artery, supply the lesser and distal greater curve, respectively. The proximal greater curve is supplied by the left gastroepiploic artery and by short gastric arteries from the splenic artery. The vessels form two extrinsic arcading anastomotic loops. The superior loop between the right and left gastric artery lies in the lesser omentum close to the lesser curve. The inferior loop between the right and left gastroepiploic lies in the greater omentum close to the greater curve. The loops give o a series of short branches to the anterior and posterior walls. The fundus and left margin of the greater curve are supplied by ®ve short gastric arteries derived from the splenic artery. The branches from the loops form a subserosal plexus.9±11 Perforating branches originating from this plexus, pass through the external muscle layers of the gastric wall to reach a richly anastomotic submucosal arterial plexus. Small side branches are given o to the external muscle layers and to Auerbach's plexus en route, but the majority of arterioles to the external muscle come from the submucosal plexus. The submucosal arterial network extends between the greater and lesser curves and provides anastomoses between the vessels derived from the lesser and those from the greater curves. The mucosa is supplied by small branches from the submucosal plexus, which pass perpendicularly through the
Vascular anatomy of the GI tract 5
OESOPHAGUS SQUAMOUS EPITHELIUM
STOMACH CN
Intraepithelial channels
MUSC. MUCOSAE SUBMUCOSA
MUSCULARIS PROPRIA SA
ADVENTITIA
SMALL INTESTINE
COLON CN
VC MUCOSA VA MUSC. MUCOSAE SUBMUCOSA
CC
SAP
CA
SAP
MUSCULARIS PROPRIA
VR VR
MA MA
Figure 3. Intramural arterial distribution in the oesophagus, stomach, small intestine and colon. Abbreviations are: CA, cryptal arteriole; CC, capillaries; CN, capillary network; MA, marginal artery; SA, supplying artery; SAP, submucosal arterial plexus; VA, villous arteriole; VC, villous capillaries; VR, vasa recta.
muscularis mucosae. In the lamina propria the arterioles branch into capillaries, which run towards the lumenal surface between the gastric glands. There are frequent cross anastomoses between adjacent capillaries. Just underneath the surface epithelium, the capillaries form a polygonal network around the necks of the gastric pits (Figure 3).12±16 Mucosal venules drain into the submucosal venous plexus, which is continuous with a similar plexus in the oesophagus and duodenum. In the gastric cardia the submucosal venous plexus is composed of a series of parallel veins oriented towards the oesophagogastric junction. Drainage of the muscle layers occurs to the submucosal venous plexus and partly to perforating veins, which pass to subserosal veins. The latter drain to arcading veins in the omenta and towards the portal system.
6 K. Geboes et al
The small intestine The duodenum is supplied chie¯y by the pancreaticoduodenal artery o the coeliac trunk. The jejunum and the ileum are supplied by a dozen branches o the superior mesenteric artery. These branches divide and anastomose several times in the mesentery, forming arcades. The last of these forms a marginal artery along the small intestine. The marginal artery is de®ned as the artery closest to, and parallel with, the wall of the intestine. From the marginal artery, blood reaches the intestine by way of short, straight branches or `vasa recta'. In the upper jejunum there are only one or two arcades and the vasa recta are 3±5 cm long. Arcades increase in number up to ®ve towards the distal ileum and the vasa recta become short. The vasa recta penetrate the external muscle layers of the bowel wall to reach a profusely anastomotic submucosal arterial plexus from which arterioles originate for the mucosa, submucosa and muscular layers. The submucosal plexus gives o two types of mucosal branches: long or villous arterioles and short or cryptal ones. Arterioles to the villi pass without branching into the lamina propria. At the tip of the villus the arteriole splays into a network of capillaries that subsequently course down along the sides of the villus in a fountain-like pattern. The crypts receive their arterial supply adjacent to the muscularis mucosae. The lymphoid tissue of the small intestine is supplied by the submucosal plexus through interfollicular arteries between the lymphoid follicles and through follicular arterioles originating from the interfollicular arteries. In Peyer's patches, some of the follicular arterioles directly supply a domelike capillary network beneath the epithelium overlying the follicles. Venous drainage of each of the small intestinal capillary beds passes to the submucosal venous plexus, which anastomoses both longitudinally and circumferentially in the bowel wall. This plexus is drained by short veins, which penetrate the external muscle layers, chie¯y along the mesenteric margin and then pass to branches of the superior mesenteric vein in the mesentery. The superior mesenteric vein receives venous drainage of the distal duodenum, the jejunum, ileum, appendix and caecum, the ascending and transverse colon and a right gastro-epiploic vein draining the stomach, before joining the splenic vein to form the hepatic portal vein.12,14,17 The large intestine Ascending and transverse colon are supplied by three branches of the superior mesenteric artery (ileocolic and right and middle colic arteries), whereas the splenic ¯exure, descending colon and sigmoid are nourished by branches of the inferior mesenteric artery (left colic and sigmoid arteries). These vessels form arcades that are less numerous and less complex than those in the small intestine. Within 2 cm of the colon wall, a single large anastomotic marginal artery is formed. This marginal artery runs retroperitoneally, extending from the ileocaecal junction down to and into the sigmoid mesocolon close to its attachment to the colon wall, thus forming an anastomotic channel between ileocolic, right, middle and left colic and sigmoid arteries. The rectum has a richly anastomosing arterial system derived from the inferior mesenteric and internal iliac arteries. Through the superior rectal artery it forms an anastomosis with the marginal artery of the colon. Short vasa recta pass from the marginal artery to the colon wall, with few or no anastomoses en route. Upon reaching the wall, they divide to form subserosal branches that pass circumferentially around the bowel wall and other branches that form a subserosal anastomosing plexus. The subserosal plexus gives o branches that traverse the external muscle coat to
Vascular anatomy of the GI tract 7
reach the submucosal arterial plexus. There is extensive anastomosis in the submucosa both longitudinally and circumferentially. Arteriolar branches from the submucosal plexus penetrate the muscularis mucosae and then break up in a chain of capillaries. These capillaries ascend along the glands and reach the surface of the mucosa where they form a honeycomb pattern around the openings of the glands, just beneath the surface epithelium. The muscularis contains capillaries derived from both the subserosal and submucosal plexuses and is perforated by larger arteries coming from the serosa and subserosa. The venous drainage largely parallels the arterial supply.12,18 The pancreas The arterial supply consists of variable branches from the coeliac trunk and the superior mesenteric artery. Arterial arcades are formed between the major supply arteries, and there are numerous anastomoses within the substance of the pancreas. Within the pancreas the arterial branches form an interlobular plexus in the connective tissue of the interlobular septa. From these plexuses single intralobular arteries pass into each lobule where they form glomerula-like tufts supplying individual islets of Langerhans and then continue to adjacent acini. Thus, a portal type of system is formed where the exocrine pancreas receives blood rich in islet-cell hormones. The veins in the pancreas correspond in general to the arterial pattern. They drain into the portal venous system behind the neck of the pancreas.19 The liver The portal vein is formed by the union of the superior mesenteric and splenic veins, and delivers blood to the liver through the hilum. This vein then progressively divides into smaller terminal branches that supply about 70% of oxygen to the liver parenchyma. The arterial blood is supplied by the hepatic artery. The right lobe of the liver is supplied by the right hepatic artery. The left lobe draws its blood from several sources. The lateral segment derives its supply from the left hepatic artery. The quadrate lobe (medial segment of the left lobe) obtains its arterial blood predominantly from the middle hepatic artery. Small branches from the left hepatic artery can augment this. Blood for the caudate lobe usually comes from the right hepatic artery, but in some instances, left or even middle hepatic arteries contribute. Once the hepatic arteries have penetrated the hepatic parenchyma, they arborize in the portal tracts alongside the portal vein and form two plexuses before delivering their blood into the liver sinusoids. One plexus is around small portal vein radicles and the other around small bile ducts. From the terminal portal veins and hepatic arterioles sprout small side branches that feed directly into the hepatic sinusoids where blood from both sources mixes in the intercommunicating complex of sinusoids. These are unique vessels lined by fenestrated endothelial cells without tight junctions and phagocytic Kuper cells. Sinusoids drain slowly into terminal hepatic veins. These join up to form the main hepatic veins that empty into the inferior vena cava just below its junction with the right atrium.20 The extramural splanchnic circulation The coeliac trunk The coeliac trunk is a short (2 cm) large (5±8 mm) artery that arises from the front of the aorta, usually at the twelfth thoracic±®rst lumbar vertebral level between the
8 K. Geboes et al
Figure 4. Selective angiogram of a normal coeliac trunk (a) showing the common hepatic artery (b), the right (c) and left (d) hepatic arteries, the left gastric artery (e), the splenic artery (f) and the gastroduodenal artery (g).
crura of the diaphragm. It passes horizontally forward above the upper margin of the pancreas. It divides almost immediately into three branches: the common hepatic, splenic and left gastric arteries (Figure 4). There are however many variations of the typical origin. The most striking of these is a common origin of the coeliac trunk and the superior mesenteric artery in a coeliacomesenteric trunk (in approximately 2% of cases). In this situation a single artery is the sole source of vascularization of the supramesocolic organs. Collateral ¯ow is only possible from the inferior mesenteric, phrenic, oesophageal and retroperitoneal arteries.9
The hepatic artery The common hepatic artery arises on the right side of the coeliac trunk and runs superiorly along the upper border of the head of the pancreas forward and to the right, giving o branches to the stomach, duodenum and pancreas. Where the gastroduodenal artery branches o, it becomes the hepatic artery proper. This artery enters the porta hepatis to the right with the hepatic duct lying to its right and the portal vein behind and divides into the right, left and middle hepatic artery. In approximately 18% of patients the hepatic artery does not originate from the coeliac trunk but emerges partially or entirely from the superior mesenteric artery. The hepatic artery is termed `replaced' when there is no other artery from the coeliac trunk supplying the same liver lobe. It is termed `accessory' when it occurs in addition to one from the coeliac trunk.
Vascular anatomy of the GI tract 9
The cystic artery typically arises to the right of the common hepatic duct from the right hepatic artery but has another origin in about 20% of cases. Reaching the gallbladder, it divides into a super®cial and a deep branch, the former being distributive to the peritoneal surface and the latter to the non-peritoneal surface of the gallbladder. Variations in the pattern of the hepatic arterial blood supply are extremely frequent. The right gastric artery is a small branch that arises from the common hepatic or left hepatic artery in about equal proportions (40%) and less frequently from the gastroduodenal artery (8%) or the middle or right hepatic artery (5%). It descends to the pylorus along the lesser curvature of the stomach where it usually anastomoses with the left gastric artery. The right gastric artery frequently gives rise to the supraduodenal artery (of Wilkie). The gastroduodenal artery usually arises from the common hepatic artery (75%) but may arise from the left or right hepatic artery or superior mesenteric artery. It descends behind the ®rst part of the duodenum anterior to the pancreas and courses to the left where it divides into the right gastroepiploic and the anterior superior pancreaticoduodenal arteries. In the majority of instances (90%) it gives rise to the `retroduodenal artery', which provides the blood supply to the common bile duct. Behind the intrapancreatic portion of the common bile duct, this artery anastomoses with the posterior inferior pancreaticoduodenal artery to form the pancreaticoduodenal arcade supplying the posterior surface of the entire duodenum and the head of the pancreas. The anterior pancreaticoduodenal arcade is formed behind the head of the pancreas by the anastomosis between the anterior superior pancreaticoduodenal artery and the anterior inferior pancreaticoduodenal artery, which arises from the superior mesenteric artery. The right gastroepiploic artery is the ®nal continuation of the gastroduodenal artery. After supplying one or more branches to the pylorus, it passes to the left along the greater curvature of the stomach. Ascending branches supply the greater curvature of the stomach and anastomose with descending branches of the right and left gastric arteries. The right gastroepiploic artery is also involved in the posterior omental arcade (Barkow) formed by the right epiploic (arising from the right gastroepiploic) and left epiploic (arising from the left gastroepiploic, a branch of the splenic artery) arteries. Branches from the omental arcade anastomose with branches from the middle and left colic, inferior pancreaticoduodenal and transverse pancreatic arteries. The left gastric artery The left gastric artery courses upwards to the left toward the gastric cardia, where it turns sharply downward and, following the lesser curvature, descends to the right toward the pylorus. It supplies part of the stomach and the inferior oesophagus. The anastomosis with the right gastric artery may be absent. In 25% of cases the left gastric artery gives rise to an aberrant left hepatic artery. The splenic artery The splenic artery arises from the coeliac artery, takes a short loop to the right, and then courses to the left along the cephalic border of the pancreas to supply the spleen. It gives o branches to the pancreas and stomach. The ®rst large pancreatic branch is the dorsal pancreatic artery, which in approximately 40% of the cases arises from the ®rst portion of the splenic artery but in 60% from other sources such as the right
10 K. Geboes et al
hepatic, superior mesenteric or coeliac arteries. The dorsal pancreatic artery descends and supplies branches to the posterior surface of the pancreas and gives o the transverse pancreatic artery, which courses to the left to supply the body and tail. The dorsal pancreatic artery gives o two branches to the right. One is joining the anterior superior pancreaticoduodenal, the gastroduodenal, or the right gastroepiploic artery and the other supplies the uncinate process. Often, a fourth branch of the dorsal pancreatic artery descends below the inferior border of the pancreas to communicate with the superior mesenteric artery. Occasionally, this branch gives rise to the middle colic artery (artery of Riolan). The arteria pancreatica magna arises from the second segment of the splenic artery and joins the transverse pancreatic artery. The caudal pancreatic arteries, which are often multiple, arise from the third and fourth segments of the splenic artery. They enter the tail of the pancreas and join branches of both, the arteria pancreatica magna and the transverse pancreatic artery. The latter may arise either from the superior mesenteric artery or the gastroduodenal artery. The left gastroepiploic artery arises from the splenic artery prior to its terminal divisions or from a terminal division itself. It courses downward to the right in the great omentum along the greater curvature of the stomach. It gives o the left epiploic artery that anastomoses with the right epiploic artery, a branch of the right gastroepiploic artery, to form the arcus epiploicus magnus of Barkow, in the great omentum below the colon. Short gastric arteries originate from the distal splenic artery and supply the fundus and cardia of the stomach. Superior mesenteric artery The superior mesenteric artery originates from the aorta at the level of the ®rst lumbar vertebra, behind the body of the pancreas. It emerges from under the lower border of the pancreas, passes forward anteriorly over the upper border of the third portion of the duodenum and descends anteriorly into the mesentery. Usually, the middle colic artery arises from the superior mesenteric artery just before it enters the mesentery. The middle colic artery can arise as a separate branch or be derived from a common right colic-middle colic trunk (53% of the cases). Occasionally, it arises directly from the coeliac artery. When the middle colic artery has a large branch running parallel and posterior to it in the transverse mesocolon, this branch is often described as the arc of Riolan. The right colic artery can arise directly (38%) from the superior mesenteric artery. The middle and right colic arteries supply the right half of the transverse colon and the ascending colon. Within the mesentery, the superior mesenteric artery courses to the right iliac fossa, curving to the left to end in the ileocolic artery by forming an anastomosis. Major side branches of the superior mesenteric artery originating usually on the right side are the inferior pancreaticoduodenal arteries supplying the lower part of the duodenum. In approximately 60% of cases there are two inferior pancreaticoduodenal arteries, but in 40% there is only one common inferior pancreaticoduodenal artery. These arteries connect with the superior pancreaticoduodenal arteries. The inferior pancreaticoduodenal artery can also arise from, or in common with, the ®rst jejunal artery. To the left, 4±6 jejunal arteries, and 9±13 intestinal branches that supply the ileum can be identi®ed. These are often called `intestinal arteries'. They divide into two branches, forming a ®rst order arcading anastomosis with the neighbouring branches. Subsequent anastomoses form second- to fourth-order arcades. Branches of these arcades ®nally form the marginal artery. The marginal artery may thus be composed of arteries that range
Vascular anatomy of the GI tract 11
Figure 5. Selective superior mesenteric angiogram showing the main branches to small bowel and right colon: (a) superior mesenteric artery, (b) jejunal arteries, (c) ileal arteries, (d) ileocolic artery, (e) right colic artery, (f) middle colic artery.
from third- or fourth-order arcades to the parent colic artery itself. The middle colic artery is often the marginal artery for the major portion of its distribution. Fine branches originating from the marginal artery reach the bowel wall as `vasa recta'. The vasa recta of the small intestine are shorter, closer together and less straight in appearance than the large bowel vasa recta. The terminal branch of the superior mesenteric artery is the ileocolic artery. It distributes branches to the terminal ileum, the caecum and the lower third or half of the ascending colon (Figure 5). In its distal distribution the ileal and colic branches of the ileocolic artery often form an `ileocolic loop'. The anterior and posterior caecal arteries and the appendicular artery arise separately from this loop. Inferior mesenteric artery The inferior mesenteric artery arises from the aorta anteriorly at the level of the third lumbar vertebra and descends to the left (Figure 6). Major side branches are the left colic artery and the sigmoidal arteries. The descending branch of the inferior mesenteric artery becomes the superior rectal artery. The left colic artery is usually an ascending branch from the inferior mesenteric artery. This branch bifurcates at the splenic ¯exure, its right branch joining the middle colic artery from the superior
12 K. Geboes et al
Figure 6. Selective angiogram of the inferior mesenteric artery showing the main branches of the left colon: (a) inferior mesenteric artery, (b) ascending branch, (c) marginal artery, (d) vasa recta, (e) descending branch and (f) sigmoid artery.
mesenteric artery and its left branch joining the marginal artery. Sigmoidal arteries can originate from the ascending branch in common with the left colic, or arise from a descending branch of the inferior mesenteric artery. A few sigmoidal arteries may arise from a middle branch. The number of sigmoid arteries varies from one to ®ve. The superior rectal artery divides into two branches of unequal size at the level of the second or third sacral vertebra, commonly at the bottom of the pouch of Douglas. The larger right branch divides into several branches that descend on the posterior and lateral surface of the rectal ampulla. The smaller, left branch deviates to the left and supplies the lateral and anterior surface. In contrast to the small and large intestinal arteries, the branches of the rectal arteries do not form arcades but enter the gut wall directly and independently. The branches of the superior rectal artery further anastomose with the middle and inferior rectal arteries originating, respectively, from the internal iliac and pudendal arteries.9±11 Venous drainage The venous blood from the gastrointestinal organs and spleen is drained by the hepatic portal circulation through the liver before it returns to the heart. The hepatic portal vein is formed by the union of the superior mesenteric and splenic veins. The superior
Vascular anatomy of the GI tract 13
mesenteric vein drains blood from the pancreas, the stomach, the small intestine and portions of the large intestine through the pancreaticoduodenal, right gastroepiploic, jejunal, ileal, ileocolic, right and middle colic veins. The splenic vein drains blood from the stomach, pancreas and portions of the large intestine through the short gastric, left gastroepiploic, pancreatic and inferior mesenteric veins. The inferior mesenteric vein, which passes into the splenic vein, drains portions of the large intestine through the superior rectal, sigmoidal and left colic veins. The right and left gastric veins, which open directly into the hepatic portal vein, drain large portions of the stomach. The cystic vein, which drains the gallbladder, also opens into the hepatic portal vein. COLLATERAL BLOOD SUPPLY The various pathways can be subdivided into six categories: channels between the coeliac trunk and the superior mesenteric artery; between the coeliac trunk and the aorta; between the dierent coeliac branches; between superior mesenteric branches; connections between the superior and inferior mesenteric artery; routes between the inferior mesenteric artery and parietal branches of the aorta. SUMMARY The blood supply of the gastrointestinal system has been studied extensively. Both the intramural and extramural vascular supply and their variants are well known. The arterial blood supply to the oesophagus is complex. The upper third is supplied by the inferior thyroid arteries, the mid third by intercostal and bronchial arteries and branches from the aorta and the lower third by the left gastric and phrenic arteries. There are anastomoses among the various components. The arterial supply of the stomach is provided by branches of the coeliac trunk. The small intestine is supplied primarily from the superior mesenteric artery and the colon is provided by branches from the superior and inferior mesenteric arteries. There are many collaterals between the dierent systems. The venous return largely parallels the arterial supply. REFERENCES
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