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 Summary
Cancer; Surgery remains the most radical method of treatment of many solid tumors, including
Colon; colorectal cancer; in these tumors, surgery is the only method that can offer the chance of
Rectum; cure. To avoid early postoperative morbidity (mainly, anastomotic leak) and to achieve
Colorectal; good long-term results (low incidence of tumor recurrence, long overall and disease-free
Surgery; survival, and optimal quality of life), the surgeon should have an in-depth knowledge of
Resection; vascular anatomy of the colon and rectum. This essential requirement is based on the fact
Radical; that the actual course followed by lymph fluid drainage from any part of the colon/rectum
Colectomy; is determined by its blood supply; therefore, the extent of resection for colorectal cancer
Arteries; follows the principles of blood supply and lymphatic drainage. Knowledge of the colorectal
Lymphatics; vascular anatomy and its variations is of vital importance in the planning of radical surgical
Lymph nodes; treatment and in appropriately performing colorectal resections, particularly in the
Veins 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. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244
2. Embryology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244
3. Applied surgical vascular anatomy of the colon and rectum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244
3.1. Arteries supplying the colon . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244
3.1.1. SMA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244
3.1.2. IMA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 246
3.2. Arteries supplying the rectum. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 247
3.2.1. Superior rectal artery. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 247

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
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244 G.H. Sakorafas et al.

3.2.2. Middle rectal arteries. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 247

3.2.3. Inferior rectal arteries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 248
3.2.4. Middle sacral artery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 248
3.3. Collateral blood supply to the colon and rectum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 248
3.3.1. Collateral circulation between celiac artery and SMA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 248
3.3.2. Collateral circulation between SMA and IMA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 249
3.3.3. Collateral blood flow between IMA and branches of the aorta–hypogastric collateral branches . . . 250
3.3.4. Adequacy of collateral circulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 250
3.4. Venous drainage of the colon and rectum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 251
3.5. Lymphatic drainage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 251
3.5.1. Colon . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 251
3.5.2. Rectum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 252
4. Comments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 252
4.1. ‘‘High’’ versus ‘‘low’’ ligation of the IMA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 252
4.2. Surgery for colorectal cancer in patients with AAA or who underwent in the past AAA repair. . . . . . . . . . 253
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 254

1. Introduction segmental artery gives rise to the celiac artery that supplies
the foregut (which includes the region extending between
Radical surgical resection remains the basic method of the esophagus and the distal duodenum), the thirteenth
treatment of many solid tumors, and offers the greatest artery gives rise to the superior mesenteric artery (SMA) to
chance for cure, especially when malignant disease has not supply the midgut (which corresponds to the intestinal
disseminated. An in-depth knowledge of the anatomy is a segment between the proximal duodenum and the mid-
basic requirement for the surgeon to optimize early and late transverse colon), and the 21st or 22nd artery gives rise to
results of surgery for malignant disease and to achieve not the inferior mesenteric artery (IMA) to supply the hindgut
only low morbidity and mortality rates following even [2,3].
complicated surgical procedures, but also prolonged overall
and disease-free survival, without recurrence of the tumor, 3. Applied surgical vascular anatomy of the
thereby ameliorating patients’ quality-of-life. colon and rectum
Colorectal cancer represents the third most common type
of cancer both in males as well as in females (excluding skin 3.1. Arteries supplying the colon
cancer); it accounts for 10% and for 11% of all types of
cancers in men and women, respectively [1]. Colorectal
In the healthy state, the colon derives its blood supply from
cancer surgery represents a large part of the daily routine in
branches of the SMA and the IMA [2–4] (Fig. 1). The rectum
many departments of surgery around the world. As is well
and anal canal are supplied by branches of the IMA and the
known, the extent of surgical resection, but also the
internal iliac arteries [4].
radicality in colorectal cancer surgery, specifically regarding
the extent of lymphadenectomy, is closely related to
vascular anatomy of the colon and rectum. Therefore, a 3.1.1. SMA
thorough knowledge of the vascular anatomy of colon and The SMA forms the central axis around which the intestines
rectum and the associated pattern of collateral variation is a rotate during embyogenesis [5]. The right colon—that is,
mandatory prerequisite for colorectal resections. The aim of the cecum, ascending colon, hepatic flexure, and proximal
this work is to summarize and critically analyze currently half or two thirds of the transverse colon—represents part
available data regarding the vascular anatomy of the colon of the embryonic midgut and is therefore supplied by
and rectum, from the perspective of a surgical oncologist. 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
2. Embryology emerges from the undersurface of the pancreas to cross
the third part of the duodenum. Consequently, the SMA runs
The formation of the aorta begins at the 3rd week of between the two layers of the small bowel mesentery, giving
embryologic development, when two strands of cells off right and left branches supplied the whole of the small
migrate dorsally from the endocardial mesenchyme and intestine and the midgut portion of the large intestine [6].
elongate caudally along the neural groove to become the The right branches include the inferior pancreaticoduodenal
dorsal aortas. These two dorsal aortas remain separate from artery (which loops upward to communicate with the
approximately 1 week but eventually fuse to form a single- pancreatoduodenal arcade), the middle colic artery, the
aortic trunk that descends caudally. The mesenteric arteries right colic artery, and the ileocolic artery. Of these,
originate from the primitive ventral segmental arteries. As the ileocolic is the most constant, as the right colic and
development proceeds, there is regression of all but three of the middle colic could be absent (see below). The left
these primitive communications, with only the precursors to branches, which number 15–20, are the jejunal (4–6) and
the three major mesenteric vessels remaining. The 10th the ileal (11–14) branches [7–9].
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Applied vascular anatomy of the colon and rectum 245

3.1.1.1. Middle colic artery. The middle colic artery is the have been described including aberrant origin from the
first branch of the SMA; it arises from the concave surface of celiac artery, IMA, common or right hepatic, right gastro-
the SMA, just inferior to the uncinate process of pancreas epiploic, gastroduodenal, dorsal or transverse pancreatic,
and just before it enters the mesentery of the small bowel, and splenic artery [10]. Anatomic variations of the middle
and supplies the transverse colon, forming a significant colic artery include complete absence in a significant
series of arcades [5,6]. It also communicates with branches percentage of individuals (up to 25%), presence of an
of the IMA. Multiple variant origins of the middle colic artery 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, approxi-
mately 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 ascend-
ing 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
Figure 1 Superior and inferior mesenteric arteries. 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]).
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246 G.H. Sakorafas et al.

communicates with the right branch of the middle colic 3.1.1.3. Ileocolic artery. The terminal branch of the SMA is
artery and the ileocolic artery, respectively. Anastomosis the ileocolic artery, which is the most constant tributary
between the right colic and ileocolic arteries is absent in 5% leaving the SMA. The ileocolic artery can be readily
of subjects. identified and used as an important landmark for angio-
graphic 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 construct-
ing 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
Figure 3 Some common variations in the blood supply to the changed to the superior rectal (or hemorrhoidal) artery (see
cecum and right colon. C, origin of the right colic artery (in below). Branches of the IMA include the left colic artery, the
black) from the ileocolic. D, origin of the right colic artery from sigmoid branches, and the superior rectal artery [9].
the middle colic. E, origin of the right colic artery from the The relationship of the ureters to the main IMA (and
superior mesenteric artery. F, absence of right colic artery. Note superior rectal artery, see below) is of particular importance
that in both E and F the right colic flexure is supplied by the for the surgical oncologist. Owing to the deviation of the
middle colic artery (from Ref. [15]). 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]).
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Applied vascular anatomy of the colon and rectum 247

Figure 5 Anatomy of the IMA and its upper branches and Figure 6 Branching patterns of the left colic artery. Type 1: A
ligation of the IMA in the course of rectal excision. (A) ‘‘Low’’ left colic artery (LCA) arising from the IMA (58%). Type 2: LCA
ligation, after the origin of left colic artery, at the level of and a first sigmoidal artery (SA) having a common trunk (27%).
aortic bifurcation. (B) ‘‘High’’ ligation, flush with the aorta LCA and SA arising simultaneously from the IMA (15%).
(from Ref. [12]).

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 The main arteries of the rectum include the superior,
not exposed to risk during this maneuver [12]. middle, and inferior rectal arteries.

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 3.2.1. Superior rectal artery
inferior mesenteric vein. Usually, it runs upward and may The superior rectal (or hemorrhoidal) artery is the terminal
reach the splenic flexure (where it bifurcates) in 85% of (descending) branch of the IMA. It typically continues the
cases [5] (Fig. 5). Typically, the right (ascending) branch downward course of IMA in the base of the vertical limb of
of the left colic artery supplies the distal third of the sigmoid mesocolon to reach the back of the upper end of the
transverse colon and the splenic flexure; it joins the rectum, where it bifurcates into two vessels, adjacent to
left branch of the middle colic artery, but a significant the inferior portion of the pouch of Douglas and opposite the
degree of variability exists in the collateral vessels in the level of S3 (though the level of bifurcation shows consider-
splenic flexure (see below, ‘‘Collateral blood supply to the able individual variation) [12]. The right branch of the
colon and rectum’’). In 15% of subjects, the middle colic superior rectal artery is larger than the left and is typically
artery is the predominant blood supply to the splenic considered as the continuation of the IMA; it supplies mainly
flexure. In the absence of a prominent left colic artery, the posterior and lateral surfaces of the rectum. The smaller
branches of the colosigmoid artery and the paracolic artery left branch, which is regarded as a collateral branch of the
may form an anastomotic arcade supplying collateral to the IMA, supplies the anterior (ventral) surface of the rectum.
splenic flexure, which has been termed the meandering The right branch divides into two main branches, which run
artery of Moskowitz or the marginal artery of Drummond down the right anterior and right posterior aspects of the
(see below, ‘‘Collateral blood supply to the colon and rectum, while the left branch continues undivided down the
rectum’’) [16,17]. left lateral aspect. These branches descend on the rectal
wall, each one generally breaking up into smaller branches
3.1.2.2. Sigmoid arteries. The sigmoid arteries typically that penetrate the muscle coat to reach the submucosa in
arise from the ascending branches of the IMA (in common which they proceed downward as straight vessels, which run
with the left colic artery) if the base of the mesocolon is in the columns of Morgagni and terminate usually above the
wide. When the base of the mesocolon is narrow, the anal valves as a capillary plexus [5].
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 3.2.2. Middle rectal arteries
2 to 9 and their precise arrangement is also very variable. These spring from the anterior divisions of the internal iliac
They anastomose each other and to the descending branch arteries or –rarely- from their inferior vesical branches and
of the left colic artery to form a series of arcades [6]. No proceed medially and forward below the pelvic peritoneum,
useful purpose will be served in describing their detailed in the tissue of the lateral ligaments to reach the rectal wall
anatomy further except to say that they communicate freely where they anastomose with the branches of the superior
by marginal arcades (Fig. 6) [12]. A collateral arcade and inferior hemorroidal vessels. However, their arrange-
between the sigmoid arteries and the superior rectal artery ment is very variable and the middle hemorrhoidal artery
is grossly visible in 50% of cases [16]. may be absent, double or treble on one or both sides [5,12].
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248 G.H. Sakorafas et al.

3.2.3. Inferior rectal arteries of the three major mesenteric arteries are compromised
These are derived indirectly from the internal iliac arteries [21]. Indeed, in chronic ischemia, usually two or more of the
through their internal pudendal branches. They leave the main trunks are occluded before symptoms of ischemia
pudendal arteries as they are lying in Alcock’s canal in the become apparent. Angiography is a useful diagnostic tool to
fascia or the outer walls of the ischiorectal fossa and run evaluate vascular patters of the colon. However, normally,
medially and slightly forward breaking up into branches collateral vessels may not be clearly visible on angiography,
which penetrate the external and internal anal sphincters but these vessels have the potential to increase in size
and reach the submucosa and subcutaneous tissues of the in response to an ischemic stimulus to maximize the blood
anal canal. They communicate with branches from the flow [5].
inferior rectal arteries of the opposite side and possibly from Specifically regarding colon and rectum, the collateral
the middle rectal arteries of both sides, leaving a potentially communications are between: (I) the celiac artery and SMA,
vessel-deficient area in the dorso-caudal sector of the rectal (II) the SMA and IMA, (III) the IMA and branches of the
ampulla [12,15]. This could explain why most anastomotic internal iliac arteries, and (IV) the visceral and parietal
leaks are observed in the dorso-caudal ampulla after low branches of the aorta [9].
anterior resection of the rectum [15].

3.2.4. Middle sacral artery 3.3.1. Collateral circulation between celiac artery and
This artery arises from the back of the aorta, just above its SMA
bifurcation and descends beneath the peritoneum on the The primary potential pathway of collateral flow between
anterior surface of the lower two lumbar vertebrae, the the celiac axis and SMA is through the gastroduodenal and
sacrum and the coccyx and behind the aorta, the left pancreaticoduodenal arteries, forming the pancreaticoduo-
common iliac vein, the presacral nerves, the superior rectal denal arterial arcade (superior pancreaticoduodenal artery
vessels, and the rectum [12]. It sends several very small from the gastroduodenal artery and inferior gastroduodenal
ranches to the posterior wall of the rectum. Some of its artery from the SMA) [20–22]. The potential communications
terminal branches may even descent along the anococcygeal may be altered dramatically, for example, when the
raphe of the levator muscle to reach the anal canal and gastroduodenal artery arises from the SMA rather than the
rectum. The practical significance of the middle sacral celiac axis. Other types of anatomic variations or collaterals
artery to the surgeon is that during rectal excision, it is between celiac artery and SMA include the branches of the
regularly exposed as the rectum is lifted off the front of the middle colic and the dorsal pancreatic arteries (from splenic
sacrum from above and is divided when the coccyx is artery), aberrant vessels (such as a replaced right hepatic
disarticulated from below, sometimes giving rise to trouble- artery), a middle colic artery arising from the celiac axis, or
some bleeding [12]. However, troublesome bleeding during a common origin of celiac artery and SMA from the aorta
rectal excision is most commonly of venous origin. (the so-called celiacomesenteric trunk). An uncommon, but
Although the superior rectal arteries provide the main well-described communication is the arc of Bühler, a direct
arterial supply to the rectum, it is quite wrong to discount communication between the celiac artery and SMA, which
almost completely the contribution made by the middle and represents a remnant of the embryonic ventral segmental
inferior rectal arteries. Indeed, experience with sphincter- arteries of the primitive intestinal vessels (Fig. 7) [4,5,9,23].
saving procedures for carcinomas of the upper/middle This collateral vessel is present in less than 2% of cases and
rectum shows that after division of the inferior mesen- may be present as a direct communication between the
teric/superior rectal trunks, the middle and inferior rectal celiac artery and the SMA [23]. It can provide immediate
arteries are capable of nourishing a distal rectal stump up collateral flow if the celiac artery or SMA becomes occluded
even up to 7–10 cm above the peritoneal reflection [12]. proximal to the origin of this arcade (Fig. 7) [5]. Although
Even when the lateral ligaments have been completely these collaterals or anatomic variations may be of impor-
divided, sacrificing the middle rectal supply, a rectal stump tance in upper GI or HPB surgery (they can provide blood
up to just below the peritoneal reflection usually has a good flow to the liver and stomach when the celiac artery is
blood supply, as shown by satisfactory arterial bleeding from occluded), they are typically of no clinical significance
its cut upper end. during surgery for colon cancer.
The epiploic arcade (the so-called arc of Barkow) is a rich
collateral network of collateral vessels between celiac
3.3. Collateral blood supply to the colon and artery and SMA [23]. The arc of Barkow lies within the
rectum greater omentum and is formed from anastomoses of the
right and left epiploic arteries (which are branches of
The mesenteric circulation has a rich system of collateral the right and left gastroepiploic arteries, derived from the
communications via collateral arcades formed among the gastroduodenal and splenic arteries, respectively) [5]. Also,
major abdominal vessels. These collateral vessels provide a the arc of Barkow receives blood supply from posterior
potential mechanism for maintaining adequate perfusion to epiploic arteries from the transverse pancreatic artery and
abdominal organs (including colon and rectum) when major tributaries from the middle colic artery. Because of its rich
mesenteric branches are surgically ligated (as during surgery vascularity within the omentum, the arc of Barkow provides
for colorectal cancer) or are critically stenotic or occluded collateral additional blood supply to numerous organs
(i.e. due to severe atherosclerotic disease) [18–20]. Because adjacent to the greater omentum, including transverse
of the abundance of potential collateral sources, ischemic colon through multiple small branches [24]. However, the
alterations of the intestines are observed when at least two significance of these collaterals is limited for the surgical
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Applied vascular anatomy of the colon and rectum 249

Figure 7 The arc of Buhler in this schematic representation, it

connects the common hepatic artery and the superior mesen-
teric 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
Figure 8 The collateral vessels between SMA and IMA:
branches.
marginal artery of Drummond, the arc of Riolan, and the
meandering artery of Moskowitz (from Ref. [5]).
oncologist who is planning a colon resection for colon
cancer.
marginal artery of Drummond remains small in cali-
ber, but it can enlarge markedly when the IMA or
3.3.2. Collateral circulation between SMA and IMA SMA is occluded. This marginal artery can provide
These collaterals are of paramount importance for the blood supply to the entire left colon in case of occ-
surgical oncologist. The basic collateral networks between lusion of IMA. Indeed, aortography showed that in
SMA and IMA are the following (Fig. 8) [5]: patients with peripheral artery disease IMA may
be blocked, and yet the sigmoid vessels fill satis-
(i) The marginal artery of Drummond: This is the major factorily, presumably through the superior mesenteric/
collateral arcade between the two mesenteric vessels, middle colic, and marginal arteries. As is well known, in
is located within the mesentery of the colon and reconstruction of abdominal aortic aneurysms (AAA) it
lies about 2–3 cm from the mesenteric border of the is regular practice to ligate the IMA at its origin, without
bowel [5,12]. From it, the ultimate branches of ill effect on the colon. As is well known from clinical
supply to the colon, the vasa recti, are distributed. practice, after ligation of the IMA flush with the
This collateral network is composed of branches abdominal aorta in the course of rectal excision, the
from the ileocolic and right, middle, left colic, and blood supply through the middle colic and marginal
sigmoidal arteries [25]. The marginal artery is usually a artery is perfectly adequate to nourish the left colon in
continuous artery that runs parallel to the colon. the vast majority of cases.
The marginal artery is better developed in the left (ii) The arc of Riolan: The arc of Riolan represents a set of
colon and is inconsistent or poorly developed in the collateral branches located centrally within the me-
right colon in 25–75% of patients [22]. There are 2 sentery and forms a communication between the
weeks or watershed points: the Grifith’s point at the middle colic and left colic arteries in a region which
splenic flexure where branches of the middle colic and usually does not have major blood vessels (Fig. 8) [13].
left colic meet, and the less important Sudek’s point It is present in about 7–10% of population.
where the last sigmoid branch and the superior (iii) The meandering artery of Moskowitz: It courses along
hemorrhoidal artery meet (Fig. 1) [9]. These points, the base of the colonic mesentery. It represents a
especially the one at the splenic flexure, are fre- connection between the proximal segment of the
quently the sites affected in segmental ischemic colitis. middle colic artery and the ascending branch of
In the absence of mesenteric arterial occlusion, the 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 tively (a branch of the internal iliac artery), and forming the
Mosckowitz, because some investigators believe that it inferior mesenteric and hypogastric collateral communica-
represents a dilated arc of Riolan, while others believe tions [5,9]. Branches of the IMA also communicate with
that it is a separate discrete anastomotic channel. The branches of the aorta by the middle sacral artery (see
meandering artery of Moskowitz dilates enormously above), which emerges from the aortic bifurcation and
when a significant arterial occlusion is present. Whether descends toward the coccyx, anastomosing to the superior
the meandering artery is discovered on a preoperative and middle rectal arteries, which originate from the IMA and
arteriogram or is palpated intraoperatively, its presence internal iliac artery, respectively [5]. In addition, collateral
implies that an occlusion (or severe stenosis) of either formation is present between vessels of the IMA and the
the SMA or IMA is present (Figs. 9A and B). If an aorta or aortic branches, like external iliac, femoral,
operation on the left colon is planned and the mean- obturator, internal pudendal, medial and lateral femoral
dering mesenteric artery is discovered, the surgeon circumflex, gluteal, deep circumflex iliac, and lumbar
must abandon his plans for a major (high) mesenteric arteries, and occasionally the celiac axis in cases of aberrant
resection or the meandering mesenteric artery, by middle colic origin [13]. These anastomoses may be
necessity, will be divided and ligated. This may cause important after surgical interruption or atherosclerotic
necrosis of the right colon and the entire small intestine occlusion of the vascular supply of the left colon and may
if the flow in the meandering mesenteric artery is maintain the viability of the gastrointestinal tract in the
retrograde (IMA to SMA) or it may cause necrosis of the presence of total occlusion of all main visceral trunks [9].
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 exclu- 3.3.4. Adequacy of collateral circulation
sion for aneurysmal disease. 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
3.3.3. Collateral blood flow between IMA and branches of more hazardous because of poorer blood supply. Weight for
the aorta–hypogastric collateral branches weight, the colon has less blood flow than other parts of the
The IMA forms collateral networks with the internal iliac gastrointestinal tract [26]. Active colonic peristalsis, which
artery, which originates from the common iliac artery. These increases intraluminal pressure, also reduces blood supply
collateral vessels consist of the superior rectal artery from [10]. The regional distribution of blood flow through
the IMA and the middle and inferior rectal arteries, arising collateral vessels can explain the preferential development
from the internal iliac artery and pudendal artery, respec- of ischemic colon injury in two mainly regions of the colon
 ARTICLE IN PRESS
Applied vascular anatomy of the colon and rectum 251

and rectum, the Griffith’s and the Sudeck’s critical points, common in clinical practice, and it not associated with
which are anatomically vulnerable to tissue ischemia problems due to ischemia.
following surgical interruption of major arterial branches
of the colon and/or rectum:
3.4. Venous drainage of the colon and rectum

(i) The Griffith’s point. This corresponds to the collateral The veins of the colon closely accompany the corresponding
communication between SMA and IMA, at the junction arteries and require little comment. They reach the portal
of the mid- and hind-gut vessels, near the splenic flexure vein by superior or inferior mesenteric tributaries. The veins
of the colon. At this point (Griffith’s point), the from the right colon open into the superior mesenteric vein,
continuity of the marginal artery may be interrupted which lies to the right of the SMA, and eventually joins the
in as many as 5–7% of individuals [27]. Inadequacy of the splenic vein to form the portal vein behind the neck of the
marginal artery in this region may compromise the pancreas. From the left colon, the veins drain to the inferior
blood supply to the splenic flexure or descending colon mesenteric vein, which lies to the left of the IMA and
from the middle colic artery if the IMA is ligated (for continues upward for 5–8 cm above the origin of the latter to
example, during surgery for AAA or for colon cancer). end by joining the splenic vein [5,12].
Diminished blood supply to this area can be observed in Veins from the upper two-thirds of the rectum are drained
up to 30% of individuals. For these reasons, in clinical by the superior rectal vein, which empties into the portal
practice, many surgeons—following ligation of the left system via the inferior mesenteric vein. Veins from the
colic or IMA—avoid making anastomoses in the region of lower third of the rectum are drained by the middle and
splenic flexure for fear that the blood supply will not be inferior rectal veins, which empty into the systemic venous
sufficient to permit healing of the anastomosis, a circulation via the internal iliac veins [31]. The venous
situation that could lead to anastomotic leak and sepsis drainage of the rectum can explain why tumors of the lower
[28,29]. The surgeon should always keep in his/her mind rectum and/or anal canal can give directly systemic (i.e.,
that the origin of the middle colic artery may be from pulmonary) metastases without hepatic metastases and
the SMA or branches of the celiac artery, and therefore moreover why rectal varices may be formed in patients
supply to the splenic flexure may depend on the with portal hypertension, complicating surgery for rectal
integrity of the more proximal vasculature, rather than cancer.
the more common blood supply from the IMA. If a
meandering anastomotic artery is present, it should be 3.5. Lymphatic drainage
preserved [9].
(ii) The Sudeck’s point. As above noted, collateral flow 3.5.1. Colon
between the systemic and visceral circulation takes The lymphatics responsible for drainage of the colon could
place through small vessels that join the superior rectal be considered as being arranged in two closely connected
artery (a branch of the IMA) to the middle rectal groups—the intramural and the extramural lymphatics.
arteries, an area known as Sudeck’s point (Fig. 1) [30]. 3.5.1.1. The intramural lymphatics. Throughout the colon
When the IMA is occluded (by atheroma) or ligated there are continuous lymphatic plexuses in the submucous
during surgery, the viability of the low sigmoid and and subserous layers of the bowel wall. These begin as blind-
rectum is maintained by collaterals from the hypogas- ended capillaries in the mucosa, and progressively larger
tric branches. Interestingly, the absence of an extra- vessels connect with lymphatic networks in the submucosa,
mural marginal artery does not preclude a functional muscularis externa, and subserosa. These are connected and
collateral circulation via intramural communications. In drain into the extramural lymphatics.
an extensive injection study of cadavers, Michels et al. 3.5.1.2. The extramural lymphatics. These consist of the
[13] concluded that the superior rectal artery can be lymphatic channels and regional lymph nodes that accom-
perfused either from above, through the marginal pany the colic blood vessels (see below) [32]. Therefore, the
artery via intramural plexuses, or from below, via the actual course followed by lymph drainage from any part of
middle and inferior rectal arteries. Perfusion was the colon is determined by its blood supply. Numerous lymph
possible even when no grossly visible anastomosis nodes are intercalated in the lymph stream of the collecting
between the superior rectal and the sigmoid artery vessels. The lymph nodes could be divided arbitrary into
was observed. In performing low anterior resections four groups—the epicolic, paracolic, intermediate and
for rectal cancer, ligation of the IMA and lateral principal nodes [12]. The epicolic lymph nodes lie on the
ligaments would compromise blood supply of the colon itself, the paracolic nodes along the marginal artery
rectum and this explain why Goh et al. have pro- between it and the colon, the intermediate nodes along the
posed to keep a short rectal stump to avoid anastomotic main colic vessels and their branches, and the principal
ischemia and breakdown [9]. At the present time, nodes on the superior and inferior mesenteric vessels.
when it is generally accepted that ligation of the In general, lymph drains from the various parts of the colon
inferior mesenteric vessels through an abdominal ap- to regional lymph nodes. Lymph from the appendix and
proach is desirable in rectal excision, and purely sacral cecum drains to ileocolic nodes via appendicular and cecal
excisions are no longer employed, Sudeck’s thesis lymphatic vessels [6]. Efferent lymphatics from the ileocolic
regarding a critical point in the marginal circulation of nodes carry lymph to the superior mesenteric lymph nodes
the rectosigmoid region has ceased to be relevant. [14]. Lymphatic vessels from the ascending colon and right
Indeed, the construction of anastomoses in this area is half of the transverse colon likewise transmit lymph to
 ARTICLE IN PRESS
252 G.H. Sakorafas et al.

groups of nodes, which are named for branches of the SMA 4. Comments
that supply the particular segment (i.e., ileocolic, right
colic, and middle colic). The lymph then passes to superior The exact extent of colonic resection is largely determined
mesenteric nodes [14]. The left half of the transverse colon, by the blood vessels that require division in order to remove
the descending colon, and the sigmoid colon drain to groups the lymphatic drainage of the tumor-bearing part of the
of lymph nodes associated with branches of the IMA, i.e. colon; the potential presence of nodal metastases requires
sigmoid nodes and left colic nodes. Lymph fluid from these high ligation of the arterial and venous supply of the colon
nodes passes to inferior mesenteric nodes [14,32]. Of note, [33]. The more radical the surgeon is in dealing with the
lymphatics draining the transverse colon communicate with lymphatic drainage, the greater the length of colon that will
those of the greater omentum and can also drain into nodes need to be resected [34]. There are few reports of
at the hilum of the spleen. However, this is a quite controlled studies to assist the surgeon in making these
exceptional route of lymphatic spread of colon cancer. decisions, and inevitably there are differences of opinion
There is no communication between the lymph vessels of regarding as to how extensive should be the resection. As a
the transverse colon and those of the stomach [6]. general rule, the extent of resection required for cancers in
After the regional lymph nodes, lymph flow follows the different parts of the colon is determined by necessity by
course of the superior or inferior mesenteric lymph nodes, the need to achieve wide resection of the extramural
along the SMA and IMA. From these nodes, lymph is lymphatics, which accompany the main colic vessels
channeled upward to the celiac nodes, the terminal lymph supplying the segment involved. Obviously, knowledge of
nodes for the subdiaphragmatic alimentary tract down to the colonic vascular anatomy and its variations is crucial to
the middle of rectum [14]. The abdominal confluence appropriate resection, particularly when a patient has had
of lymph trunks joins the paired lumbar lymph trunks to previous aortic or colonic surgery [35]. The surgeon should
form the thoracic duct. Sometimes, lymph fluid misses be cognizant of the patient’s vascular anatomy, particularly
the regional (epicolic, paracolic, and intermediate nodes) in patients who had a colectomy that has changed the usual
and is drained directly to the principal lymph nodes pattern of collateral blood supply to the colon [35]. Radical
on the superior or inferior mesenteric vessels (‘‘skip’’ colon resection should achieve not only complete excision of
metastases). 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
3.5.2. Rectum colorectal cancer, only two pertinent points will be briefly
As in the colon, lymphatics responsible for the drainage of commented: the level of ligation of the IMA (high vs. low
lymph fluid from the rectum could be considered as being in ligation) and surgical resections in patients with AAA or who
two closely connected groups—the intramural and the underwent in the past AAA repair.
extramural lymphatics.

3.5.2.1. The intramural lymphatics. Throughout the rec- 4.1. ‘‘High’’ versus ‘‘low’’ ligation of the IMA
tum there are continuous lymphatic plexuses in the
submucous and subserous layers of the bowel wall, which The issue of ‘‘high’’ vs. ‘‘low’’ ligation of IMA has been a
are connected and drain into the extramural lymphatics. highly controversial topic since the turn of the 20th century
(Fig. 10). ‘High’’ ligation of the IMA (defined as ligation of
3.5.2.2. The extramural lymphatics. In general, these this vessel at the point where the artery springs from the
follow the blood vessels supplying the rectum and anal abdominal aorta, under cover of the 3rd part of the
canal. Lymph from the upper third of the rectum, which duodenum) is preferred by many surgeons, no matter where
receives its blood supply from the superior rectal artery, the tumor is sited in the left colon [34]. At least
drains to superior rectal nodes after transversing para- theoretically, ‘‘high’’ ligation of the IMA could improve the
rectal nodes. From superior rectal nodes, lymph passes lymphatic clearance, and seems to be a reasonable
superiorly to inferior mesenteric nodes. The lymphatic extension of the operation, albeit being associated with a
drainage of the remainder of the rectum and anal canal higher risk of hypogastric nerve injury [44]. The inferior
is dependent on its relation to the mucocutaneous junc- mesenteric vein is ligated by a separate ligature at about
tion. The part proximal to the mucocutaneous junction the same level or even higher. ‘‘High’’ ligation of the IMA
either drains superiorly, parallel to the middle rectal means that the perfusion of the left part of the transverse
artery and its branches on the corresponding side wall of colon (which is used to construct the anastomosis) is based
the pelvis, or traverses the levator ani muscle to follow on the middle colic artery; at the same time, the main blood
the inferior rectal artery; both pathways lead to in- supply to the rectum through the superior rectal artery is
ternal iliac nodes, common iliac nodes, and the lumbar interrupted, and any part of the distal colon retained below
trunks [14]. Lymphatic drainage from the anal canal the tumor have to be nourished entirely by the middle and
inferior to the mucocutaneous junction is exceptional in inferior rectal vessels. The experience of many surgeons
that it does not parallel blood vessels. The collecting shows that this latter supply is certainly sufficient to
ducts pass anteriorly and superiorly in the perineum; maintain a viable condition of the upper rectum and
together with lymphatic channels from perianal skin, they rectosigmoid for a distance up to 10 cm above the peritoneal
pass to superficial inguinal nodes. Lymph from superficial reflection off the front of the rectum, but it would probably
inguinal nodes makes its way to the lumbar trunks via be unwise to rely on it to supply any greater extent of bowel
external iliac nodes [14]. [44]. Clearly, therefore, when the more radical step of
 ARTICLE IN PRESS
Applied vascular anatomy of the colon and rectum 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
Figure 10 Point of division of the IMA during resection for rectal arteries. A careful review of operative notes describ-
rectosigmoid carcinomas. (A) ‘‘High’’ ligation of the IMA ing the previous operation is mandatory to understand the
involves division of the IMA at its origin from the aorta. (B) changes regarding arterial supply of the colon. Similar
‘‘Low’’ ligation of the IMA preserves the left folic artery.

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 contra-
indicated in older or poor-risk patients [44].

Figure 11 Correct (A) and incorrect (B) methods of ligating

4.2. Surgery for colorectal cancer in patients with the IMA near its origin from an abdominal aortic aneurysm
AAA or who underwent in the past AAA repair (AAA). If ligature is too far distal, it interrupts critical collateral
flow from the left colic to sigmoid branches of the IMA. It is
As is well known, in patients with AAAs, the IMA is often usually safest to oversew the IMA origin from within the open
occluded or severely stenosed due to severe atheromatous AAA (from Ref. [56]).
 ARTICLE IN PRESS
254 G.H. Sakorafas et al.

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