Applied vascular anatomy of the colon and rectum: Clinical implications for the surgical oncologist

ARTICLE IN PRESS Surgical Oncology (2006) 15, 243–255

Available at www.sciencedirect.com

journal homepage: www.elsevier.com/locate/suronc

REVIEW

Applied vascular anatomy of the colon and rectum: Clinical implications for the surgical oncologist George H. Sakorafas, Efstratios Zouros, George Peros 4th Department of Surgery, Athens University, Medical School, Attikon University Hospital, Athens, Greece Accepted 14 March 2007

KEYWORDS Cancer; Colon; Rectum; Colorectal; Surgery; Resection; Radical; Colectomy; Arteries; Lymphatics; Lymph nodes; Veins

Summary Surgery remains the most radical method of treatment of many solid tumors, including colorectal cancer; in these tumors, surgery is the only method that can offer the chance of cure. To avoid early postoperative morbidity (mainly, anastomotic leak) and to achieve good long-term results (low incidence of tumor recurrence, long overall and disease-free survival, and optimal quality of life), the surgeon should have an in-depth knowledge of vascular anatomy of the colon and rectum. This essential requirement is based on the fact that the actual course followed by lymph fluid drainage from any part of the colon/rectum is determined by its blood supply; therefore, the extent of resection for colorectal cancer follows the principles of blood supply and lymphatic drainage. Knowledge of the colorectal vascular anatomy and its variations is of vital importance in the planning of radical surgical treatment and in appropriately performing colorectal resections, particularly in the patient who underwent in the past colectomy or aortic surgery that has changed the usual pattern of collateral blood supply to the colon. This review summarizes currently available data regarding vascular anatomy of the colon and rectum, from a surgical perspective. & 2007 Elsevier Ltd. All rights reserved.

Contents 1. 2. 3.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Embryology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Applied surgical vascular anatomy of the colon and rectum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Arteries supplying the colon . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.1. SMA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.2. IMA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Arteries supplying the rectum. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.1. Superior rectal artery. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Corresponding author. Arkadias 19–21, GR-115 26 Athens, Greece. Tel.: +30 210 74 87 318; fax: +30 210 74 87 192.

E-mail address: [email protected] (G.H. Sakorafas). 0960-7404/$ - see front matter & 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.suronc.2007.03.002

244 244 244 244 244 246 247 247

ARTICLE IN PRESS 244

4.

G.H. Sakorafas et al. 3.2.2. Middle rectal arteries. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.3. Inferior rectal arteries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.4. Middle sacral artery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Collateral blood supply to the colon and rectum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.1. Collateral circulation between celiac artery and SMA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.2. Collateral circulation between SMA and IMA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.3. Collateral blood flow between IMA and branches of the aorta–hypogastric collateral branches . . . 3.3.4. Adequacy of collateral circulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. Venous drainage of the colon and rectum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5. Lymphatic drainage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5.1. Colon . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5.2. Rectum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Comments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. ‘‘High’’ versus ‘‘low’’ ligation of the IMA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Surgery for colorectal cancer in patients with AAA or who underwent in the past AAA repair. . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction Radical surgical resection remains the basic method of treatment of many solid tumors, and offers the greatest chance for cure, especially when malignant disease has not disseminated. An in-depth knowledge of the anatomy is a basic requirement for the surgeon to optimize early and late results of surgery for malignant disease and to achieve not only low morbidity and mortality rates following even complicated surgical procedures, but also prolonged overall and disease-free survival, without recurrence of the tumor, thereby ameliorating patients’ quality-of-life. Colorectal cancer represents the third most common type of cancer both in males as well as in females (excluding skin cancer); it accounts for 10% and for 11% of all types of cancers in men and women, respectively [1]. Colorectal cancer surgery represents a large part of the daily routine in many departments of surgery around the world. As is well known, the extent of surgical resection, but also the radicality in colorectal cancer surgery, specifically regarding the extent of lymphadenectomy, is closely related to vascular anatomy of the colon and rectum. Therefore, a thorough knowledge of the vascular anatomy of colon and rectum and the associated pattern of collateral variation is a mandatory prerequisite for colorectal resections. The aim of this work is to summarize and critically analyze currently available data regarding the vascular anatomy of the colon and rectum, from the perspective of a surgical oncologist.

2. Embryology The formation of the aorta begins at the 3rd week of embryologic development, when two strands of cells migrate dorsally from the endocardial mesenchyme and elongate caudally along the neural groove to become the dorsal aortas. These two dorsal aortas remain separate from approximately 1 week but eventually fuse to form a singleaortic trunk that descends caudally. The mesenteric arteries originate from the primitive ventral segmental arteries. As development proceeds, there is regression of all but three of these primitive communications, with only the precursors to the three major mesenteric vessels remaining. The 10th

247 248 248 248 248 249 250 250 251 251 251 252 252 252 253 254

segmental artery gives rise to the celiac artery that supplies the foregut (which includes the region extending between the esophagus and the distal duodenum), the thirteenth artery gives rise to the superior mesenteric artery (SMA) to supply the midgut (which corresponds to the intestinal segment between the proximal duodenum and the midtransverse colon), and the 21st or 22nd artery gives rise to the inferior mesenteric artery (IMA) to supply the hindgut [2,3].

3. Applied surgical vascular anatomy of the colon and rectum 3.1. Arteries supplying the colon In the healthy state, the colon derives its blood supply from branches of the SMA and the IMA [2–4] (Fig. 1). The rectum and anal canal are supplied by branches of the IMA and the internal iliac arteries [4]. 3.1.1. SMA The SMA forms the central axis around which the intestines rotate during embyogenesis [5]. The right colon—that is, the cecum, ascending colon, hepatic flexure, and proximal half or two thirds of the transverse colon—represents part of the embryonic midgut and is therefore supplied by branches of the SMA [6]. In less than 1% of cases, the origin of SMA fuses with the celiac artery, creating a common vessel, the so-called celiacomesenteric trunk [5]. SMA emerges from the undersurface of the pancreas to cross the third part of the duodenum. Consequently, the SMA runs between the two layers of the small bowel mesentery, giving off right and left branches supplied the whole of the small intestine and the midgut portion of the large intestine [6]. The right branches include the inferior pancreaticoduodenal artery (which loops upward to communicate with the pancreatoduodenal arcade), the middle colic artery, the right colic artery, and the ileocolic artery. Of these, the ileocolic is the most constant, as the right colic and the middle colic could be absent (see below). The left branches, which number 15–20, are the jejunal (4–6) and the ileal (11–14) branches [7–9].

ARTICLE IN PRESS Applied vascular anatomy of the colon and rectum 3.1.1.1. Middle colic artery. The middle colic artery is the first branch of the SMA; it arises from the concave surface of the SMA, just inferior to the uncinate process of pancreas and just before it enters the mesentery of the small bowel, and supplies the transverse colon, forming a significant series of arcades [5,6]. It also communicates with branches of the IMA. Multiple variant origins of the middle colic artery

Figure 1 Superior and inferior mesenteric arteries.

245 have been described including aberrant origin from the celiac artery, IMA, common or right hepatic, right gastroepiploic, gastroduodenal, dorsal or transverse pancreatic, and splenic artery [10]. Anatomic variations of the middle colic artery include complete absence in a significant percentage of individuals (up to 25%), presence of an accessory (10%) or double middle colic artery (Fig. 2) [11–15]. When the right colic artery is absent, it is replaced by an abnormally large right colic branch. The middle colic artery is divided into a right and a left branch, approximately at the center of the transverse colon. The left branch may have independent origins including SMA, IMA, dorsal pancreatic artery and splenic artery. The left branch of the middle colic artery supplies a part of the colon also supplied by the left colic artery through the collateral channel of the marginal artery (see below, collateral blood supply). The blood supply to the splenic flexure has been shown to be variable in that it is carried by the IMA via the left colic artery in 89% of cases and by the SMA via the middle colic artery in 11%. Where the middle colic artery is absent, the splenic flexure is supplied by the right colic artery (originating from the SMA) and the left colic artery. 3.1.1.2. Right colic artery. The right colic artery—together with the ileocecal artery (see below)—supplies the ascending colon; it has the greatest variations among colic arteries (Fig. 3) [13–15]. It may arise directly from the SMA in about 40% of subjects, the middle colic in 30%, the ileocolic artery in 12%, whether it may be absent in about 20% of subjects [6]. Interestingly, in one study, a true right colic artery arising from the SMA was found in only 13% of cadavers [13]. When the right colic artery is absent, the ascending colon is supplied by the middle colic and ileocolic arteries [11]. It divides into an ascending and descending branch that

Figure 2 Common variations of the middle colic artery. G, middle colic artery (in black) almost reaches the left flexure and it is reinforced by a more direct second branch. H, middle colic artery also shifted to the left. I, accessory middle colic artery supplying the left flexure, and J, absence of middle colic artery (from Ref. [15]).

ARTICLE IN PRESS 246 communicates with the right branch of the middle colic artery and the ileocolic artery, respectively. Anastomosis between the right colic and ileocolic arteries is absent in 5% of subjects.

Figure 3 Some common variations in the blood supply to the cecum and right colon. C, origin of the right colic artery (in black) from the ileocolic. D, origin of the right colic artery from the middle colic. E, origin of the right colic artery from the superior mesenteric artery. F, absence of right colic artery. Note that in both E and F the right colic flexure is supplied by the middle colic artery (from Ref. [15]).

G.H. Sakorafas et al. 3.1.1.3. Ileocolic artery. The terminal branch of the SMA is the ileocolic artery, which is the most constant tributary leaving the SMA. The ileocolic artery can be readily identified and used as an important landmark for angiographic interpretation [5]. It provides collateral vessels to the terminal ileum, cecum, and first half of the right colon. The anterior and posterior cecal vessels arise from the ileal branch of the ileocolic artery and are distributed over the respective sides of the cecum. The posterior cecal artery is the most significant artery supplying most of the cecum (Fig. 4) [6,14,15]. It also gives off the appendicular artery [14]. The ileal branch of the ileocolic artery anastomoses with the distal end of the main stem of the SMA, and in so doing completes a loop of all the branches from the right side of this major vessel (Fig. 4A). The mesenteric arcades become modified in the last part of the terminal ileum to form a marginal vessel. This is of particular value when constructing a terminal ileostomy [6]. 3.1.2. IMA The arterial supply to the left colon is from the IMA by means of its left colic and sigmoid branches [12]. The IMA is one-half the diameter of the SMA. It originates from the front of the abdominal aorta, near its left margin, at least 4 cm above the level of aortic bifurcation, approximately 6–7 cm below the SMA, just below the third part of the duodenum, at the level of the L3 vertebrae [12]. At its origin it is frequently overlaid by the lower border of the third part of the duodenum, which has thus sometimes to be displaced slightly upward or to the right if a really high tie of this vessel flush with the aorta is being practiced in a rectal excision (Fig. 5B). From its commencement, the artery runs downward arching slightly to the left, and as it crosses the left common artery close to the aorta its name is arbitrarily changed to the superior rectal (or hemorrhoidal) artery (see below). Branches of the IMA include the left colic artery, the sigmoid branches, and the superior rectal artery [9]. The relationship of the ureters to the main IMA (and superior rectal artery, see below) is of particular importance for the surgical oncologist. Owing to the deviation of the trunk to the left, it passes close to the left ureter and left

Figure 4 (A) Anterior and posterior cecal arteries arising from a common trunk from the ileocolic artery. (B) Anterior cecal artery arising first. Both the posterior cecal and appendicular arteries arise form an arcade between the ascending colic and ileal branches (From Ref. [15]).

ARTICLE IN PRESS Applied vascular anatomy of the colon and rectum

Figure 5 Anatomy of the IMA and its upper branches and ligation of the IMA in the course of rectal excision. (A) ‘‘Low’’ ligation, after the origin of left colic artery, at the level of aortic bifurcation. (B) ‘‘High’’ ligation, flush with the aorta (from Ref. [12]).

247

Figure 6 Branching patterns of the left colic artery. Type 1: A left colic artery (LCA) arising from the IMA (58%). Type 2: LCA and a first sigmoidal artery (SA) having a common trunk (27%). LCA and SA arising simultaneously from the IMA (15%).

3.2. Arteries supplying the rectum spermatic vessels, which are in danger during ligation of the IMA; the right ureter is correspondingly farther distant and is not exposed to risk during this maneuver [12]. 3.1.2.1. Left colic artery. The left colic artery, which is the first or highest branch of the IMA, travels adjacent to the inferior mesenteric vein. Usually, it runs upward and may reach the splenic flexure (where it bifurcates) in 85% of cases [5] (Fig. 5). Typically, the right (ascending) branch of the left colic artery supplies the distal third of the transverse colon and the splenic flexure; it joins the left branch of the middle colic artery, but a significant degree of variability exists in the collateral vessels in the splenic flexure (see below, ‘‘Collateral blood supply to the colon and rectum’’). In 15% of subjects, the middle colic artery is the predominant blood supply to the splenic flexure. In the absence of a prominent left colic artery, branches of the colosigmoid artery and the paracolic artery may form an anastomotic arcade supplying collateral to the splenic flexure, which has been termed the meandering artery of Moskowitz or the marginal artery of Drummond (see below, ‘‘Collateral blood supply to the colon and rectum’’) [16,17]. 3.1.2.2. Sigmoid arteries. The sigmoid arteries typically arise from the ascending branches of the IMA (in common with the left colic artery) if the base of the mesocolon is wide. When the base of the mesocolon is narrow, the sigmoid arteries may arise from the descending branch of the IMA [5]. A few sigmoidal arteries may arise from a middle branch. The number of sigmoid arteries varies from 2 to 9 and their precise arrangement is also very variable. They anastomose each other and to the descending branch of the left colic artery to form a series of arcades [6]. No useful purpose will be served in describing their detailed anatomy further except to say that they communicate freely by marginal arcades (Fig. 6) [12]. A collateral arcade between the sigmoid arteries and the superior rectal artery is grossly visible in 50% of cases [16].

The main arteries of the rectum include the superior, middle, and inferior rectal arteries.

3.2.1. Superior rectal artery The superior rectal (or hemorrhoidal) artery is the terminal (descending) branch of the IMA. It typically continues the downward course of IMA in the base of the vertical limb of sigmoid mesocolon to reach the back of the upper end of the rectum, where it bifurcates into two vessels, adjacent to the inferior portion of the pouch of Douglas and opposite the level of S3 (though the level of bifurcation shows considerable individual variation) [12]. The right branch of the superior rectal artery is larger than the left and is typically considered as the continuation of the IMA; it supplies mainly the posterior and lateral surfaces of the rectum. The smaller left branch, which is regarded as a collateral branch of the IMA, supplies the anterior (ventral) surface of the rectum. The right branch divides into two main branches, which run down the right anterior and right posterior aspects of the rectum, while the left branch continues undivided down the left lateral aspect. These branches descend on the rectal wall, each one generally breaking up into smaller branches that penetrate the muscle coat to reach the submucosa in which they proceed downward as straight vessels, which run in the columns of Morgagni and terminate usually above the anal valves as a capillary plexus [5].

3.2.2. Middle rectal arteries These spring from the anterior divisions of the internal iliac arteries or –rarely- from their inferior vesical branches and proceed medially and forward below the pelvic peritoneum, in the tissue of the lateral ligaments to reach the rectal wall where they anastomose with the branches of the superior and inferior hemorroidal vessels. However, their arrangement is very variable and the middle hemorrhoidal artery may be absent, double or treble on one or both sides [5,12].

ARTICLE IN PRESS 248

G.H. Sakorafas et al.

3.2.3. Inferior rectal arteries These are derived indirectly from the internal iliac arteries through their internal pudendal branches. They leave the pudendal arteries as they are lying in Alcock’s canal in the fascia or the outer walls of the ischiorectal fossa and run medially and slightly forward breaking up into branches which penetrate the external and internal anal sphincters and reach the submucosa and subcutaneous tissues of the anal canal. They communicate with branches from the inferior rectal arteries of the opposite side and possibly from the middle rectal arteries of both sides, leaving a potentially vessel-deficient area in the dorso-caudal sector of the rectal ampulla [12,15]. This could explain why most anastomotic leaks are observed in the dorso-caudal ampulla after low anterior resection of the rectum [15].

of the three major mesenteric arteries are compromised [21]. Indeed, in chronic ischemia, usually two or more of the main trunks are occluded before symptoms of ischemia become apparent. Angiography is a useful diagnostic tool to evaluate vascular patters of the colon. However, normally, collateral vessels may not be clearly visible on angiography, but these vessels have the potential to increase in size in response to an ischemic stimulus to maximize the blood flow [5]. Specifically regarding colon and rectum, the collateral communications are between: (I) the celiac artery and SMA, (II) the SMA and IMA, (III) the IMA and branches of the internal iliac arteries, and (IV) the visceral and parietal branches of the aorta [9].

3.2.4. Middle sacral artery This artery arises from the back of the aorta, just above its bifurcation and descends beneath the peritoneum on the anterior surface of the lower two lumbar vertebrae, the sacrum and the coccyx and behind the aorta, the left common iliac vein, the presacral nerves, the superior rectal vessels, and the rectum [12]. It sends several very small ranches to the posterior wall of the rectum. Some of its terminal branches may even descent along the anococcygeal raphe of the levator muscle to reach the anal canal and rectum. The practical significance of the middle sacral artery to the surgeon is that during rectal excision, it is regularly exposed as the rectum is lifted off the front of the sacrum from above and is divided when the coccyx is disarticulated from below, sometimes giving rise to troublesome bleeding [12]. However, troublesome bleeding during rectal excision is most commonly of venous origin. Although the superior rectal arteries provide the main arterial supply to the rectum, it is quite wrong to discount almost completely the contribution made by the middle and inferior rectal arteries. Indeed, experience with sphinctersaving procedures for carcinomas of the upper/middle rectum shows that after division of the inferior mesenteric/superior rectal trunks, the middle and inferior rectal arteries are capable of nourishing a distal rectal stump up even up to 7–10 cm above the peritoneal reflection [12]. Even when the lateral ligaments have been completely divided, sacrificing the middle rectal supply, a rectal stump up to just below the peritoneal reflection usually has a good blood supply, as shown by satisfactory arterial bleeding from its cut upper end.

3.3.1. Collateral circulation between celiac artery and SMA The primary potential pathway of collateral flow between the celiac axis and SMA is through the gastroduodenal and pancreaticoduodenal arteries, forming the pancreaticoduodenal arterial arcade (superior pancreaticoduodenal artery from the gastroduodenal artery and inferior gastroduodenal artery from the SMA) [20–22]. The potential communications may be altered dramatically, for example, when the gastroduodenal artery arises from the SMA rather than the celiac axis. Other types of anatomic variations or collaterals between celiac artery and SMA include the branches of the middle colic and the dorsal pancreatic arteries (from splenic artery), aberrant vessels (such as a replaced right hepatic artery), a middle colic artery arising from the celiac axis, or a common origin of celiac artery and SMA from the aorta (the so-called celiacomesenteric trunk). An uncommon, but well-described communication is the arc of Bu ¨hler, a direct communication between the celiac artery and SMA, which represents a remnant of the embryonic ventral segmental arteries of the primitive intestinal vessels (Fig. 7) [4,5,9,23]. This collateral vessel is present in less than 2% of cases and may be present as a direct communication between the celiac artery and the SMA [23]. It can provide immediate collateral flow if the celiac artery or SMA becomes occluded proximal to the origin of this arcade (Fig. 7) [5]. Although these collaterals or anatomic variations may be of importance in upper GI or HPB surgery (they can provide blood flow to the liver and stomach when the celiac artery is occluded), they are typically of no clinical significance during surgery for colon cancer. The epiploic arcade (the so-called arc of Barkow) is a rich collateral network of collateral vessels between celiac artery and SMA [23]. The arc of Barkow lies within the greater omentum and is formed from anastomoses of the right and left epiploic arteries (which are branches of the right and left gastroepiploic arteries, derived from the gastroduodenal and splenic arteries, respectively) [5]. Also, the arc of Barkow receives blood supply from posterior epiploic arteries from the transverse pancreatic artery and tributaries from the middle colic artery. Because of its rich vascularity within the omentum, the arc of Barkow provides collateral additional blood supply to numerous organs adjacent to the greater omentum, including transverse colon through multiple small branches [24]. However, the significance of these collaterals is limited for the surgical

3.3. Collateral blood supply to the colon and rectum The mesenteric circulation has a rich system of collateral communications via collateral arcades formed among the major abdominal vessels. These collateral vessels provide a potential mechanism for maintaining adequate perfusion to abdominal organs (including colon and rectum) when major mesenteric branches are surgically ligated (as during surgery for colorectal cancer) or are critically stenotic or occluded (i.e. due to severe atherosclerotic disease) [18–20]. Because of the abundance of potential collateral sources, ischemic alterations of the intestines are observed when at least two

ARTICLE IN PRESS Applied vascular anatomy of the colon and rectum

Figure 7 The arc of Buhler in this schematic representation, it connects the common hepatic artery and the superior mesenteric artery, thereby constituting a direct channel for collateral circulation when stenosis of the celiac artery or SMA is present. However, this arc may connect another branch of the celiac artery (or the celiac artery itself) to the SMA or one of its branches.

oncologist who is planning a colon resection for colon cancer. 3.3.2. Collateral circulation between SMA and IMA These collaterals are of paramount importance for the surgical oncologist. The basic collateral networks between SMA and IMA are the following (Fig. 8) [5]: (i) The marginal artery of Drummond: This is the major collateral arcade between the two mesenteric vessels, is located within the mesentery of the colon and lies about 2–3 cm from the mesenteric border of the bowel [5,12]. From it, the ultimate branches of supply to the colon, the vasa recti, are distributed. This collateral network is composed of branches from the ileocolic and right, middle, left colic, and sigmoidal arteries [25]. The marginal artery is usually a continuous artery that runs parallel to the colon. The marginal artery is better developed in the left colon and is inconsistent or poorly developed in the right colon in 25–75% of patients [22]. There are 2 weeks or watershed points: the Grifith’s point at the splenic flexure where branches of the middle colic and left colic meet, and the less important Sudek’s point where the last sigmoid branch and the superior hemorrhoidal artery meet (Fig. 1) [9]. These points, especially the one at the splenic flexure, are frequently the sites affected in segmental ischemic colitis. In the absence of mesenteric arterial occlusion, the

249

Figure 8 The collateral vessels between SMA and IMA: marginal artery of Drummond, the arc of Riolan, and the meandering artery of Moskowitz (from Ref. [5]).

marginal artery of Drummond remains small in caliber, but it can enlarge markedly when the IMA or SMA is occluded. This marginal artery can provide blood supply to the entire left colon in case of occlusion of IMA. Indeed, aortography showed that in patients with peripheral artery disease IMA may be blocked, and yet the sigmoid vessels fill satisfactorily, presumably through the superior mesenteric/ middle colic, and marginal arteries. As is well known, in reconstruction of abdominal aortic aneurysms (AAA) it is regular practice to ligate the IMA at its origin, without ill effect on the colon. As is well known from clinical practice, after ligation of the IMA flush with the abdominal aorta in the course of rectal excision, the blood supply through the middle colic and marginal artery is perfectly adequate to nourish the left colon in the vast majority of cases. (ii) The arc of Riolan: The arc of Riolan represents a set of collateral branches located centrally within the mesentery and forms a communication between the middle colic and left colic arteries in a region which usually does not have major blood vessels (Fig. 8) [13]. It is present in about 7–10% of population. (iii) The meandering artery of Moskowitz: It courses along the base of the colonic mesentery. It represents a connection between the proximal segment of the middle colic artery and the ascending branch of the left colic artery [17]. Some controversy exists

ARTICLE IN PRESS 250

G.H. Sakorafas et al.

Figure 9 (A) The superior mesenteric artery (SMA) is occluded with retrograde flow in the tortuous meandering mesenteric artery, through the inferior mesenteric artery (IMA). (B) The inferior mesenteric artery (IMA) is occluded with antegrade flow in the tortuous meandering mesenteric artery through the superior mesenteric artery (From Daniel et al., Surg Gynecol Obstet 1987; 164: 487–492).

regarding the true origin of the meandering artery of Mosckowitz, because some investigators believe that it represents a dilated arc of Riolan, while others believe that it is a separate discrete anastomotic channel. The meandering artery of Moskowitz dilates enormously when a significant arterial occlusion is present. Whether the meandering artery is discovered on a preoperative arteriogram or is palpated intraoperatively, its presence implies that an occlusion (or severe stenosis) of either the SMA or IMA is present (Figs. 9A and B). If an operation on the left colon is planned and the meandering mesenteric artery is discovered, the surgeon must abandon his plans for a major (high) mesenteric resection or the meandering mesenteric artery, by necessity, will be divided and ligated. This may cause necrosis of the right colon and the entire small intestine if the flow in the meandering mesenteric artery is retrograde (IMA to SMA) or it may cause necrosis of the sigmoid colon and upper rectum if the flow is antegrade (SMA to IMA) especially if the left hypogastric artery is not patent either because of atherosclerosis or exclusion for aneurysmal disease.

3.3.3. Collateral blood flow between IMA and branches of the aorta–hypogastric collateral branches The IMA forms collateral networks with the internal iliac artery, which originates from the common iliac artery. These collateral vessels consist of the superior rectal artery from the IMA and the middle and inferior rectal arteries, arising from the internal iliac artery and pudendal artery, respec-

tively (a branch of the internal iliac artery), and forming the inferior mesenteric and hypogastric collateral communications [5,9]. Branches of the IMA also communicate with branches of the aorta by the middle sacral artery (see above), which emerges from the aortic bifurcation and descends toward the coccyx, anastomosing to the superior and middle rectal arteries, which originate from the IMA and internal iliac artery, respectively [5]. In addition, collateral formation is present between vessels of the IMA and the aorta or aortic branches, like external iliac, femoral, obturator, internal pudendal, medial and lateral femoral circumflex, gluteal, deep circumflex iliac, and lumbar arteries, and occasionally the celiac axis in cases of aberrant middle colic origin [13]. These anastomoses may be important after surgical interruption or atherosclerotic occlusion of the vascular supply of the left colon and may maintain the viability of the gastrointestinal tract in the presence of total occlusion of all main visceral trunks [9].

3.3.4. Adequacy of collateral circulation Despite the extensive collateral anastomoses between arteries of the colon and rectum, it is generally accepted that colonic, as compared to small bowel, anastomoses are more hazardous because of poorer blood supply. Weight for weight, the colon has less blood flow than other parts of the gastrointestinal tract [26]. Active colonic peristalsis, which increases intraluminal pressure, also reduces blood supply [10]. The regional distribution of blood flow through collateral vessels can explain the preferential development of ischemic colon injury in two mainly regions of the colon

ARTICLE IN PRESS Applied vascular anatomy of the colon and rectum and rectum, the Griffith’s and the Sudeck’s critical points, which are anatomically vulnerable to tissue ischemia following surgical interruption of major arterial branches of the colon and/or rectum:

(i) The Griffith’s point. This corresponds to the collateral communication between SMA and IMA, at the junction of the mid- and hind-gut vessels, near the splenic flexure of the colon. At this point (Griffith’s point), the continuity of the marginal artery may be interrupted in as many as 5–7% of individuals [27]. Inadequacy of the marginal artery in this region may compromise the blood supply to the splenic flexure or descending colon from the middle colic artery if the IMA is ligated (for example, during surgery for AAA or for colon cancer). Diminished blood supply to this area can be observed in up to 30% of individuals. For these reasons, in clinical practice, many surgeons—following ligation of the left colic or IMA—avoid making anastomoses in the region of splenic flexure for fear that the blood supply will not be sufficient to permit healing of the anastomosis, a situation that could lead to anastomotic leak and sepsis [28,29]. The surgeon should always keep in his/her mind that the origin of the middle colic artery may be from the SMA or branches of the celiac artery, and therefore supply to the splenic flexure may depend on the integrity of the more proximal vasculature, rather than the more common blood supply from the IMA. If a meandering anastomotic artery is present, it should be preserved [9]. (ii) The Sudeck’s point. As above noted, collateral flow between the systemic and visceral circulation takes place through small vessels that join the superior rectal artery (a branch of the IMA) to the middle rectal arteries, an area known as Sudeck’s point (Fig. 1) [30]. When the IMA is occluded (by atheroma) or ligated during surgery, the viability of the low sigmoid and rectum is maintained by collaterals from the hypogastric branches. Interestingly, the absence of an extramural marginal artery does not preclude a functional collateral circulation via intramural communications. In an extensive injection study of cadavers, Michels et al. [13] concluded that the superior rectal artery can be perfused either from above, through the marginal artery via intramural plexuses, or from below, via the middle and inferior rectal arteries. Perfusion was possible even when no grossly visible anastomosis between the superior rectal and the sigmoid artery was observed. In performing low anterior resections for rectal cancer, ligation of the IMA and lateral ligaments would compromise blood supply of the rectum and this explain why Goh et al. have proposed to keep a short rectal stump to avoid anastomotic ischemia and breakdown [9]. At the present time, when it is generally accepted that ligation of the inferior mesenteric vessels through an abdominal approach is desirable in rectal excision, and purely sacral excisions are no longer employed, Sudeck’s thesis regarding a critical point in the marginal circulation of the rectosigmoid region has ceased to be relevant. Indeed, the construction of anastomoses in this area is

251 common in clinical practice, and it not associated with problems due to ischemia.

3.4. Venous drainage of the colon and rectum The veins of the colon closely accompany the corresponding arteries and require little comment. They reach the portal vein by superior or inferior mesenteric tributaries. The veins from the right colon open into the superior mesenteric vein, which lies to the right of the SMA, and eventually joins the splenic vein to form the portal vein behind the neck of the pancreas. From the left colon, the veins drain to the inferior mesenteric vein, which lies to the left of the IMA and continues upward for 5–8 cm above the origin of the latter to end by joining the splenic vein [5,12]. Veins from the upper two-thirds of the rectum are drained by the superior rectal vein, which empties into the portal system via the inferior mesenteric vein. Veins from the lower third of the rectum are drained by the middle and inferior rectal veins, which empty into the systemic venous circulation via the internal iliac veins [31]. The venous drainage of the rectum can explain why tumors of the lower rectum and/or anal canal can give directly systemic (i.e., pulmonary) metastases without hepatic metastases and moreover why rectal varices may be formed in patients with portal hypertension, complicating surgery for rectal cancer.

3.5. Lymphatic drainage 3.5.1. Colon The lymphatics responsible for drainage of the colon could be considered as being arranged in two closely connected groups—the intramural and the extramural lymphatics. 3.5.1.1. The intramural lymphatics. Throughout the colon there are continuous lymphatic plexuses in the submucous and subserous layers of the bowel wall. These begin as blindended capillaries in the mucosa, and progressively larger vessels connect with lymphatic networks in the submucosa, muscularis externa, and subserosa. These are connected and drain into the extramural lymphatics. 3.5.1.2. The extramural lymphatics. These consist of the lymphatic channels and regional lymph nodes that accompany the colic blood vessels (see below) [32]. Therefore, the actual course followed by lymph drainage from any part of the colon is determined by its blood supply. Numerous lymph nodes are intercalated in the lymph stream of the collecting vessels. The lymph nodes could be divided arbitrary into four groups—the epicolic, paracolic, intermediate and principal nodes [12]. The epicolic lymph nodes lie on the colon itself, the paracolic nodes along the marginal artery between it and the colon, the intermediate nodes along the main colic vessels and their branches, and the principal nodes on the superior and inferior mesenteric vessels. In general, lymph drains from the various parts of the colon to regional lymph nodes. Lymph from the appendix and cecum drains to ileocolic nodes via appendicular and cecal lymphatic vessels [6]. Efferent lymphatics from the ileocolic nodes carry lymph to the superior mesenteric lymph nodes [14]. Lymphatic vessels from the ascending colon and right half of the transverse colon likewise transmit lymph to

ARTICLE IN PRESS 252 groups of nodes, which are named for branches of the SMA that supply the particular segment (i.e., ileocolic, right colic, and middle colic). The lymph then passes to superior mesenteric nodes [14]. The left half of the transverse colon, the descending colon, and the sigmoid colon drain to groups of lymph nodes associated with branches of the IMA, i.e. sigmoid nodes and left colic nodes. Lymph fluid from these nodes passes to inferior mesenteric nodes [14,32]. Of note, lymphatics draining the transverse colon communicate with those of the greater omentum and can also drain into nodes at the hilum of the spleen. However, this is a quite exceptional route of lymphatic spread of colon cancer. There is no communication between the lymph vessels of the transverse colon and those of the stomach [6]. After the regional lymph nodes, lymph flow follows the course of the superior or inferior mesenteric lymph nodes, along the SMA and IMA. From these nodes, lymph is channeled upward to the celiac nodes, the terminal lymph nodes for the subdiaphragmatic alimentary tract down to the middle of rectum [14]. The abdominal confluence of lymph trunks joins the paired lumbar lymph trunks to form the thoracic duct. Sometimes, lymph fluid misses the regional (epicolic, paracolic, and intermediate nodes) and is drained directly to the principal lymph nodes on the superior or inferior mesenteric vessels (‘‘skip’’ metastases).

3.5.2. Rectum As in the colon, lymphatics responsible for the drainage of lymph fluid from the rectum could be considered as being in two closely connected groups—the intramural and the extramural lymphatics. 3.5.2.1. The intramural lymphatics. Throughout the rectum there are continuous lymphatic plexuses in the submucous and subserous layers of the bowel wall, which are connected and drain into the extramural lymphatics. 3.5.2.2. The extramural lymphatics. In general, these follow the blood vessels supplying the rectum and anal canal. Lymph from the upper third of the rectum, which receives its blood supply from the superior rectal artery, drains to superior rectal nodes after transversing pararectal nodes. From superior rectal nodes, lymph passes superiorly to inferior mesenteric nodes. The lymphatic drainage of the remainder of the rectum and anal canal is dependent on its relation to the mucocutaneous junction. The part proximal to the mucocutaneous junction either drains superiorly, parallel to the middle rectal artery and its branches on the corresponding side wall of the pelvis, or traverses the levator ani muscle to follow the inferior rectal artery; both pathways lead to internal iliac nodes, common iliac nodes, and the lumbar trunks [14]. Lymphatic drainage from the anal canal inferior to the mucocutaneous junction is exceptional in that it does not parallel blood vessels. The collecting ducts pass anteriorly and superiorly in the perineum; together with lymphatic channels from perianal skin, they pass to superficial inguinal nodes. Lymph from superficial inguinal nodes makes its way to the lumbar trunks via external iliac nodes [14].

G.H. Sakorafas et al.

4. Comments The exact extent of colonic resection is largely determined by the blood vessels that require division in order to remove the lymphatic drainage of the tumor-bearing part of the colon; the potential presence of nodal metastases requires high ligation of the arterial and venous supply of the colon [33]. The more radical the surgeon is in dealing with the lymphatic drainage, the greater the length of colon that will need to be resected [34]. There are few reports of controlled studies to assist the surgeon in making these decisions, and inevitably there are differences of opinion regarding as to how extensive should be the resection. As a general rule, the extent of resection required for cancers in different parts of the colon is determined by necessity by the need to achieve wide resection of the extramural lymphatics, which accompany the main colic vessels supplying the segment involved. Obviously, knowledge of the colonic vascular anatomy and its variations is crucial to appropriate resection, particularly when a patient has had previous aortic or colonic surgery [35]. The surgeon should be cognizant of the patient’s vascular anatomy, particularly in patients who had a colectomy that has changed the usual pattern of collateral blood supply to the colon [35]. Radical colon resection should achieve not only complete excision of the tumor, but also a tension-free anastomosis, with good blood supply [32,36–44]. Since the aim of this paper is not to discuss the practical operative details of resection for colorectal cancer, only two pertinent points will be briefly commented: the level of ligation of the IMA (high vs. low ligation) and surgical resections in patients with AAA or who underwent in the past AAA repair.

4.1. ‘‘High’’ versus ‘‘low’’ ligation of the IMA The issue of ‘‘high’’ vs. ‘‘low’’ ligation of IMA has been a highly controversial topic since the turn of the 20th century (Fig. 10). ‘High’’ ligation of the IMA (defined as ligation of this vessel at the point where the artery springs from the abdominal aorta, under cover of the 3rd part of the duodenum) is preferred by many surgeons, no matter where the tumor is sited in the left colon [34]. At least theoretically, ‘‘high’’ ligation of the IMA could improve the lymphatic clearance, and seems to be a reasonable extension of the operation, albeit being associated with a higher risk of hypogastric nerve injury [44]. The inferior mesenteric vein is ligated by a separate ligature at about the same level or even higher. ‘‘High’’ ligation of the IMA means that the perfusion of the left part of the transverse colon (which is used to construct the anastomosis) is based on the middle colic artery; at the same time, the main blood supply to the rectum through the superior rectal artery is interrupted, and any part of the distal colon retained below the tumor have to be nourished entirely by the middle and inferior rectal vessels. The experience of many surgeons shows that this latter supply is certainly sufficient to maintain a viable condition of the upper rectum and rectosigmoid for a distance up to 10 cm above the peritoneal reflection off the front of the rectum, but it would probably be unwise to rely on it to supply any greater extent of bowel [44]. Clearly, therefore, when the more radical step of

ARTICLE IN PRESS Applied vascular anatomy of the colon and rectum

Figure 10 Point of division of the IMA during resection for rectosigmoid carcinomas. (A) ‘‘High’’ ligation of the IMA involves division of the IMA at its origin from the aorta. (B) ‘‘Low’’ ligation of the IMA preserves the left folic artery.

253 changes. Obviously, in these patients high ligation of the IMA carries little risk of inducing colon ischemia. In contrast, if ligature of the IMA is too far distal, it may interrupt critical collateral flow from the left colic to sigmoid branches of the IMA (Fig. 11) [54]. In an attempt to preserve colon arterial supply, revascularization of the IMA during AAA repair has been proposed. This technique should be used when there is absence of sufficient collateral blood flow, as determined by measuring stump pressures via the patent IMA or by sterile Doppler ultrasonography of the collateral arcades and bowel wall [55]. Revascularization of the IMA by an interposition venous graft is another method to avoid colonic ischemia during AAA repair; however, this is a less attractive option, since it is a more complicated procedure [54,55]. Obviously, these are important considerations when the surgeon is planning to perform a colon resection in patients who underwent in the past AAA repair; in these patients usually the viability of the left colon usually relies on the marginal artery and on collaterals with the SMA and middle/inferior rectal arteries. A careful review of operative notes describing the previous operation is mandatory to understand the changes regarding arterial supply of the colon. Similar

ligating the IMA at its origin is taken, the resection must be prolonged distally to ensure that the distal stump of the bowel is not too long to have an adequate blood supply. To ensure adequate perfusion of the distal rectal remnant, most surgeons make the anastomosis at the level of upper rectum in the pelvis [44]. This means that the dissection involved extends from the upper abdomen to the pelvic cavity. Obviously, this more radical form of colon resection imposes a greater strain on the patient compared to ‘‘low’’ ligation of IMA. Most studies, however, have shown that ‘‘high’’ ligation of the IMA is not associated with a significant improvement of survival compared to ‘‘low’’ ligation of IMA (defined as ligation of this vessel immediately distal to the left colic artery) when the most proximal lymph nodes were involved [45–51], even regarding long term results (up to 12 years) [48]. In contrast to the findings of most studies, an improved survival advantage of 13.8% and 5.7% was found in the study by Rosi et al. [52] and Grinell et al. [53], respectively. Based on the findings of most studies, many surgeons do not perform routinely high ligation of the IMA in the resection of rectosigmoid cancers; however, the decision should be individualized based on the particular findings of each patient [33,34]. The surgeon should acknowledge that ‘‘high’’ ligation of the IMA facilitates the construction of a tension-free anastomosis and is compulsory when a common trunk between left colic artery and first sigmoid artery exists (a variant observed in 27% of cases) [41]. Obviously, ‘‘high’’ ligation of IMA requires extended mobilization and resection of the colon/rectum, without clear advantages regarding long-term results, this type of surgery is contraindicated in older or poor-risk patients [44].

4.2. Surgery for colorectal cancer in patients with AAA or who underwent in the past AAA repair As is well known, in patients with AAAs, the IMA is often occluded or severely stenosed due to severe atheromatous

Figure 11 Correct (A) and incorrect (B) methods of ligating the IMA near its origin from an abdominal aortic aneurysm (AAA). If ligature is too far distal, it interrupts critical collateral flow from the left colic to sigmoid branches of the IMA. It is usually safest to oversew the IMA origin from within the open AAA (from Ref. [56]).

ARTICLE IN PRESS 254 considerations may be relevant for patients with bilateral iliac artery aneurysms, when IMA ligation is required. Similarly, patients with prior colectomy are at increased risk for the appearance of ischemic colitis after AAA repair, because of the interruption of collateral circulation due to previous colon surgery. In these patients careful evaluation of colonic vasculature is required either preoperatively or intraoperatively, to determine the adequacy of collateral circulation, to determine the extent of the problem, and guide the surgeon during the decision-making process. In conclusion, an in-depth knowledge of vascular anatomy of the colon and rectum (and its variations) is required from the part of the surgeon when treating patients with colorectal cancer in order to avoid severe intraoperative complications (i.e. troublesome bleeding) and early postoperative morbidity (mainly, ischemia of the anastomosis with subsequent leakage). Given that the actual course followed by lymph fluid drainage from any part of the colon/ rectum is determined by its blood supply, the extent of resection for colorectal cancer follows the principles of blood supply and lymphatic drainage. Therefore, meticulous surgical technique based on this knowledge optimizes longterm results of surgery for colorectal cancer.

References [1] Jemal A, Siegel R, Ward E, Murray T, Xu J, Smigal C, et al. Cancer Statistics 2006. CA Cancer Journal for Clinicians 2006;56:106–30. [2] Rosenblum JD, Boyle CM, Scwartz LB. The mesenteric circulation. Surgical Clinics of North America 1997;77:289–305. [3] Sadler TW. Langman’s medical embryology. Baltimore: Williams & Wilkins; 1985. [4] Rosenblum JD, Boyle CM, Schwartz LB. The mesenteric circulation. Anatomy and physiology. Surgical Clinics of North America 1997;77:289–306. [5] Lin PH, Chaikof EL. Embryology, anatomy, and surgical exposure of the great abdominal vessels. Surgical Clinics of North America 2000;80:417–33. [6] Sagar PM, Pemberton JH. Topographic anatomy. In: Nicholls RJ, Dozois RR, editors. Surgery of the colon and rectum. New York: Churchill Livingstone Eds; 1997. p. 1–18. [7] Sonneland J, Anson B, Beaton L. Surgical anatomy of the arterial supply of the colon from the superior mesenteric artery based upon a study of 600 specimens. Surgery Gynecology and Obstetrics 1958;106:385–98. [8] Stewart JA, Rankin FW. Blood supply of the large intestine: its surgical considerations. Archives of Surgery 1933;26:843–91. [9] Goh H-S. Intestinal ischemia. In: Nicholls RJ, Dozois RR, editors. Surgery of the colon and rectum. New York: Churchill Livingstone Eds; 1997. p. 1–18. [10] Michels N, Siddarth P, Kornblith P. The variant blood supply to the small and large intestines: Its importance in regional resections. Journal International College of the Surgeons 1963;39:127–33. [11] Marston A. Vascular disease of the gastrointestinal tract: pathophysiology, recognition and management, 2nd ed. Baltimore: Williams & Wilkins; 1986. p. 1–15. [12] Goligher JC. Surgical anatomy and physiology of the colon, rectum, and anus. In: Golligher JC, editor. Surgery of the anus, rectum, and colon. 2nd ed. London: Bailliere, Tindall & Cassell; 1967. p. 1–54. [13] Michels N, Siddarth P, Kornblith P. The variant blood supply to the descending colon, rectosigmoid, and rectum, based on 400 dissections. Disease of the Colon and Rectum 1965;8:251–78.

G.H. Sakorafas et al. [14] Wenk EJ. Anatomy of the small bowel, colon and rectum. In: Mazier WP, Levien DH, Luchtefeld MA, Senagore AJ, editors. Surgery of the colon, rectum and anus. Philadelphia: W.B. Saunders Co; 1995. p. 4–26. [15] Vogel P, Klosterhalfen B. The surgical anatomy of the rectal and anal blood vessels. Langenbecks Archives of Surgery 1988; 373:264–9. [16] Drummmond H. The arterial supply of the rectum and pelvic colon. British Journal of Surgery 1913;1:677–82. [17] Moskowitz M, Zimmerman H, Felson B. The meandering mesenteric artery of the colon. AJR American Journal of Roentgenology 1964;92:1088–91. [18] Skandalakis JE, Kingsnorth AN, Colborn GL, Weidman TA, Skandalakis PN, Skandalakis LJ. Surgical anatomy of the colon and rectum. In: Skandalakis JE, editor. Surgical anatomy. Athens: Paschalidis Medical Publications; 2004. p. 875–913. [19] Mahmoud N, Rombeau J, Ross HM, Fry RD. Colon and rectum. In: Townsend Jr CM, Beauchamp RD, Evers BM, Mattox KL, editors. Sabiston textbook of surgery. 17th ed. Philadelphia: Saunders WB Ed; 2004. p. 1459–64. [20] Geboes K, Geboes KP, Maleux G. Vascular anatomy of the gastrointestinal tract. Best Practice and Research Clinical Gastroenterology 2001;15(1):1–14. [21] Taylor Jr LM, Moneta GL. Intestinal ischemia. In: Porter JM, Taylor Jr LM, editors. Basic data underlying clinical decision making in vascular surgery. St Louis: Quality Medical Publishing; 1994. p. 107–10. [22] Krupski WC, Selzman CH, Whitehill TA. Unusual causes of mesenteric ischemia. Surgical Clinics of North America 1997;77:471–502. [23] Nebesar RA, Pollard JJ. A critical evaluation of selective celiac and superior mesenteric angiography. Radiology 1967;89:1017–27. [24] Barkow J. Disquisitions circa originem et decursum arteriarum mammalium. Lippsiae, 1829. [25] Kornblith PL, Boley SJ, Whitehouse BS. Anatomy of the splanchnic circulation. Surgical Clinics of North America 1992;72:1–30. [26] Drummond H. Some points relating to the surgical anatomy of the arterial supply of the large intestine. Journal of Royal Society of Medicine 1913;7:185–93. [27] Leather RP, Shah DM, Kaufman JL. Comparative analysis of retroperitoneal and transperitoneal aortic replacement for aneurysm. Surgery Gynecology and Obstetrics 1989;168:38–41. [28] Kadir S. Atlas of normal and variant angiographic anatomy. Philadelphia: WB Saunders Ed; 1991. p. 541. [29] Griffiths JD. Surgical anatomy of the blood supply of the distal colon. Annals of the Royal College of Surgeons of England 1956;19:241–56. [30] Golligher JC. The adequacy of the marginal blood supply to the left colon after high ligation of the inferior mesenteric artery during excision of the rectum. British Journal of Surgery 1954;41:351–3. [31] Sudeck P. Ueber die Gefa ¨ssversorgung des Mastdarmes in Hinsicht auf die operative Gangran. Mu ¨nchen Med Wchnschr 1907;54:1314–7. [32] Thiele JW. Colon, Rectum, and Anus. In: Crabtreee TD, editor. General Surgery. Philadelphia: Lippincott Williams & Wilkins; 2000. p. 317–42. [33] Chang GJ, Shelton AA, Welton ML. Large intestine. In: Doherty GM, editor. Current surgical diagnosis and treatment. 12th Ed. New York: Lange Medical Books/McGraw-Hill (Ed); 2006. p. 685–737. [34] Marcello PW, Schoeltz DJ. Surgery for colonic carcinoma. In: Nicholls RJ, Dozois RR, editors. Surgery of the colon and rectum. New York: Churchill Livingstone Eds; 1997. p. 411–26. [35] Williams NS. Surgical management of carcinoma of the colon and rectum, with particular reference to colon cancer. In: Keighley MRB, Williams NS, editors. Surgery of the anus, rectum, and colon. Longon: WB Saunders (Ed); 1993. p. 886–938.

ARTICLE IN PRESS Applied vascular anatomy of the colon and rectum [36] Bower TC. Ischemic colitis. Surgical Clinics of North America 1993;73:1037–53. [37] Bremmer BM, Ota DM. Adenocarcinoma of the colon and rectum. ACS Surgery Principles and Practice 2006:572–83. [38] Simmang CL, Huber PJ. Management of cancer of the colon. Current therapy in colon and rectal surgery 2005; 379–87. [39] Tagliacozzo S, Tocchi A. Extended mesenteric excision in right hemicolectomy for carcinoma of the colon. International Journal of Colorectal Disease 1997;12(5):272–5. [40] Tagliacozzo S, Accordino M, Tocchi A. Extended lymphadenectomy during resection of cancer of the right colon. European Journal of Surgery 1994;160(3 Mar):179–81. [41] Herfarth C, Runkel N. Surgical standards in primary colon cancer. Chirurg 1994;65(6 Jun):514–23. [42] Yada H, Sawai K, Taniguchi H, Hoshima M, Katoh M, Takahashi T. Analysis of vascular anatomy and lymph node metastases warrants radical segmental bowel resection for colon cancer. World Journal of Surgery 1997;21(1 Jan):109–15. [43] Yamazaki T, Shirai Y, Tada T, Sasaki M, Sakai Y, Hatakeyama K. Ischemic colitis arising in watershed areas of the colonic blood supply. Surgery Today 1997;27(5):460–2. [44] Yamazaki T, Shirai Y, Sakai Y, Hatakeyama K. Ischemic stricture of the rectosigmoid colon caused by division of the superior rectal artery below Sudeck’s point during sigmoidectomy. Surgery Today 1997;27(3):254–6. [45] Goligher JC. Scope of excision required for radical removal of carcinomas in various segments of the colon. In: Golligher JC, editor. Surgery of the anus, rectum, and colon. 2nd Ed. London: Bailliere, Tindall & Cassell; 1967. p. 522–608. [46] Pezim ME, Nicholls RJ. Survival after high or low ligation of the inferior mesenteric artery during curative surgery for rectal cancer. Annals of Surgery 1984;200:729–33.

255 [47] Surtees P, Ritchie JK, Phillips RK. High versus low ligation of the inferior mesenteric artery in rectal cancer. British Journal of Surgery 1990;77:618–21. [48] Corder AP, Karanja ND, Williams JD, Heald RJ. Flush aortic tie versus selective preservation of the ascending left colic artery in low anterior resection for rectal carcinoma. British Journal of Surgery 1992;79:680–2. [49] Rouffet F, Hay JM, Vacher B, et al. Curative resection for left colonic carcinoma: hemicolectomy vs. segmental colectomy. A prospective, controlled, multicenter trial. French Association for Surgical Research. Disease of Colon and Rectum 1994;37:651–9. [50] Adachi Y, Inomata M, Miyazaki N, et al. Distribution of lymph node metastasis and level of inferior mesenteric artery ligation in colorectal cancer. Journal of Clinical Gastroenterology 1998;26(3 Apr):179–82. [51] Dworkin MJ, Allen-Mersh TG. Effect of inferior mesenteric artery ligation on blood flow in the marginal artery-dependent sigmoid colon. Journal of the American College of Surgery 1996;183(4 Oct):357–60. [52] Rosi PA, Cahill WJ, Carey J. A ten year study of hemicolectomy in the treatment of carcinoma of the left half of the colon. Surgery Gynecology and Obstetrics 1962;114:15–24. [53] Grinnell RS. Results of ligation of inferior mesenteric artery at the aorta in resections of carcinoma of the descending and sigmoid colon and rectum. Surgery Gynecology and Obstetrics 1965;120:1031–6. [54] Toursarkissian B, Thompson RW. Ischemic colitis. Surgical Clinics of North America 1997;77:461–70. [55] Ernst CB. Colon ischemia following abdominal aortic reconstruction. In: Bernhard VM, Towne JB, editors. Complications in vascular surgery. New York: Grune & Stratton; 1980. p. 396.