Gastrointestinal Surgery Series: Colorectal Surgery Prabin Bikram Thapa, Dhiresh Kumar Maharjan
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New Insights into the Surgical Anatomy and Embryology of the Rectum: A ReviewCHAPTER 1

William Willaert,
Wim P Ceelen,
Piet Pattyn,
Yves Van Nieuwenhove


During the 3rd week of gestation, the primitive gut elongates and differentiates into foregut, midgut, and hindgut. The rectum and the upper two-thirds of the anal canal develop at the dilated caudal part of the hindgut, called the cloaca. The lower one-third of the anal canal originates from an invagination of surface ectoderm, which eventually fuses with the cloaca. Due to this dual origin, both parts have a different vascular supply. The superior rectal artery, derived from the inferior mesenteric artery, represents the main vascular supply above the levator ani muscle, while the inferior rectal arteries are dominant in the lowest part of the intestinal tract. The middle rectal arteries have a variable contribution at the watershed between these two circulations. Similarly, the levator ani muscle separates the nervous system in the lower pelvis. There is now evidence that both nervous pathways innervate this muscle in the majority of cases via both the pudendal nerve and the levator ani nerve. The rectum is surrounded by the fatty mesorectum which is enclosed by the proper rectal fascia. Recognition of the surgical planes, preservation of the anatomy of the mesorectum, and sparing of the pelvic nerves are essential to correctly perform a total mesorectal excision for rectal cancer.
This review extensively describes new insights into the embryology and surgical anatomy of the rectum. In addition, recent research about several topics in rectal cancer surgery is discussed.
• Key words: Embryology, neoplasms, colorectal surgery.  
The gastrointestinal tract develops from modifications of the primitive gut. By the 3rd week, endodermal cells have migrated around the inside 2of the blastocyst, completing a pouch called the yolk sac. The primitive gut, composed entirely of endoderm, develops early in the fourth week when the dorsal part of the yolk sac incorporates into the embryo during the process of folding. The endoderm of the yolk sac becomes the epithelium of the digestive tract. Soon thereafter, the mesoderm forms and splits into somatic and splanchnic layers. The splanchnic mesoderm associates with the endoderm of the primitive gut. The endodermal layer of the primitive gut produces the epithelial lining and glands of most of the gastrointestinal tract. The vascular portion, smooth muscle, connective tissue, and parietal peritoneum develop from somatic mesoderm. Visceral peritoneum develops from splanchnic mesoderm.
The primitive gut elongates and, at about the latter part of the third week, it differentiates into an anterior foregut, a central midgut, and a posterior hindgut. The distal third of the transverse colon, the descending colon, the sigmoid colon, the rectum, and the anal canal above the dentate line are all derived from the hindgut. Therefore, this segment is supplied by the hindgut (inferior mesenteric) artery with corresponding venous and lymphatic drainage.1
The rectum and the upper two-thirds of the anal canal develop at the dilated caudal part of the hindgut, called the cloaca. This cavity is well-defined at 3rd week of gestation. It receives the allantoic diverticulum and mesonephric duct.2 At 5th week of gestation, the cloaca differentiates into twp separate organ systems—the urogenital tract and the anorectal tract.3
The proctodeum or anal pit, formed between the 5th and 10th weeks of gestation, is an invagination of surface ectoderm that fuses with the hindgut and develops into the lower one-third of the anal canal.1
A thorough knowledge of the anatomy of the hindgut and lower anal canal is essential for any surgeon performing colorectal procedures.
By convention, the rectum originates at the end of the sigmoid colon at the sacral promontory and ends below the coccyx. The transition from sigmoid colon to rectum occurs with the cessation of the teniae coli and appendices epiploicae. Anteriorly and superiorly, the rectum is covered by peritoneum, however, the majority of the rectum is extraperitoneal.4 The rectum is arbitrarily divided into three parts: The low rectum (upto 6 cm from the anal verge), the mid rectum (from 7–11 cm), and the upper rectum (from 12–15 cm).
The anal canal starts a few centimeters proximal to the dentate line and ends at the anal verge. The anal canal varies from 2–5 cm in length.5
Arterial Supply to the Hindgut
During embryologic development primitive ventral segmental arteries at the level of the aortic trunk give rise to the inferior mesenteric artery 3(IMA). The IMA arises from the ventral abdominal aorta, near its left margin, at least 4 cm above the level of aortic bifurcation. The artery goes down to the left passing close to the left ureter and left spermatic/ovarian vessels.6, 7
The IMA gives off the left colic artery that runs alongside the inferior mesenteric vein to the splenic flexure and extends to the midtransverse colon in 15%–20% of cases. In 15% of subjects, the middle colic artery is the predominant blood supply to the splenic flexure.6, 8, 9
If the base of the mesocolon is wide, the sigmoid arteries typically arise from the ascending branches of the IMA in common with the left colic artery. When the base of the mesocolon is narrow, the sigmoid arteries may arise from the descending branch of the IMA.8 A few sigmoid arteries may arise from a middle branch. The number of sigmoid arteries and their arrangement is highly variable. They interconnect with each other and communicate with the descending branch of the left colic artery forming a series of arcades.10 A collateral arcade between the sigmoid arteries and the superior rectal artery (SRA) is visible in half of cases.11
The SRA is the terminal descending branch of the IMA. It descends in the base of the vertical limb of the sigmoid mesocolon and continues downward in the mesorectum, where it bifurcates into two vessels, adjacent to the inferior portion of the pouch of Douglas and opposite the level of S3. The level of bifurcation varies. The larger right branch supplies the posterior and lateral surfaces of the rectum. The smaller left branch provides blood to the anterior surface of the rectum.6, 8 There exists a good network of small artery collaterals based on the SRA and its bifurcation in the upper and midmesorectum.12
Arterial Supply to the Lower Anal Canal
The middle rectal arteries (MRA) arise from the internal iliac arteries and reach the rectal wall passing the lateral attachments of the rectum where they anastomose with the branches of the SRA and inferior rectal arteries (IRA). The frequency of appearance of the MRA varies.2, 6, 8, 1316
The IRA derives from the internal pudendal artery and passes through Alcock's canal medially and slightly forward, and provides blood to the anal sphincters and epithelium. This vessel communicates with branches from the IRA of the opposite side and possibly from the MRA of both sides, leaving a potentially vessel-deficient area in the dorsocaudal portion of the rectal ampulla.6 In addition, a poor network of small artery collaterals based solely on variable intramural collaterals in the lower rectum might help explain the higher leak rate after low anterior resection in the posterior aspect of the short rectal stump.12
Generally, the SRA and its branches represent the dominant vascular supply above the levator muscle whereas the IRA is dominant below the levator muscle and the MRA has a variable contribution at the watershed between these two circulations.124
Collateral blood supply to the rectum
  1. Collateral circulation between the superior mesenteric artery SMA and IMA (Fig. 1.1):
    The marginal artery of Drummond (named after Sir David Drummond (1852–1932), an English physician) is the major collateral arcade between the two mesenteric vessels; located within the mesocolon about 2.5 cm from the mesocolic border of the colon, it gives the vasa recta to the colon.6, 8 Some pass only as far as the mesocolic aspect (vasa recta brevia) and some pass as far as the antimesocolic aspect on the bowel wall (vasa recta longa). Collaterals between the vasa recta occur both extramurally on the bowel wall as well as intramurally. At the splenic flexure and the proximal and middescending colon, the vasa recta are spaced 2 cm apart and have few collaterals.12 This arcade is complete in only 15%–20% of people.17 It can enlarge markedly when the SMA or IMA is occluded. In case of occlusion or surgical interruption of the base of the IMA the middle colic and marginal colic arteries adequately supply the left colon in the vast majority of cases. 6, 18
    The arc of Riolan (named after the French anatomist Jean Riolan, 1577–1657) is a second centrally located network within the mesocolon connecting the middle colic and left colic arteries.
    zoom view
    Figure. 1.1: The collateral vessels between SMA and IMA
    It is present in about 7%–10% of the population.6,8,19
    The third potential collateral pathway, the meandering artery of Moskowitz, courses along the base of the mesocolon. It is a connection between the proximal segment of the middle colic artery and the ascending branch of the left colic artery.9 Some controversies exist regarding the true origin of this artery, because some investigators believe that it represents a dilated arc of Riolan, while others believe that it is a separate discrete anastomotic channel.6,8
  2. Collateral blood flow between IMA and branches of the internal iliac artery:
    These collateral vessels consist of the SRA derived from the IMA and the MRA and IRA, arising from the internal iliac artery.6,8
  3. Branches of the IMA also communicate with branches of the aorta via the middle sacral artery which emerges 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 and the sacrum towards the coccyx. On its course the artery gives several very small branches to the posterior wall of the rectum and the anal canal. The middle sacral artery is of importance to the surgeon because it is regularly exposed as the rectum is lifted off the front of the sacrum, sometimes giving rise to troublesome bleeding.
    Collateral formation is also present between vessels of the IMA and other 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 case of aberrant middle colic origin.6,8 These collateral pathways may be important in case of surgical interruption or atherosclerotic occlusion of the vascular supply of the left colon.6
    The Griffith's critical point, located at the splenic flexure of the colon, corresponds to the collateral communication between SMA and IMA. Because at this point the continuity of the marginal artery may be interrupted in as many as 5%–7% of individuals, it is anatomically vulnerable to tissue ischemia following surgical interruption of major arterial branches of the colon and/or rectum. Moreover, infrequent occurrence of vasa recta at the splenic flexure and the proximal to mid-descending colon also contribute to vulnerability to tissue ischemia.12
    The Sudeck's critical point regarding the marginal circulation of the rectosigmoid region has ceased to be relevant.6
Venous Drainage of the Left Colon and Rectum
Veins from the left colon drain into the inferior mesenteric vein, which lies to the left of the IMA and ascends in the retroperitoneal plane and continues posterior to the pancreas to join the splenic vein.6,176
The venous drainage of the rectum parallels the arterial supply. The superior rectal veins drain the upper and middle-thirds of the rectum. They empty into the portal system via the inferior mesenteric vein. The middle rectal veins drain the lower rectum and the upper anal canal into the internal iliac vein. The inferior rectal veins drain the lower anal canal into the internal pudendal vein, and subsequently into the internal iliac vein.20
Lymphatic Drainage
Lymphatic drainage of the rectum parallels the vascular supply, therefore, the extent of resection for colorectal cancer follows the principles of blood supply and lymphatic drainage.6
The intramural lymphatic plexuses in the submucous and subserous layers of the rectal wall drain into the extramural lymphatics. The latter follows the blood vessels supplying the rectum and anal canal.6 In the mesorectum, the majority of lymph nodes are located within the posterior upper two-thirds.21
Lymphatic drainage of the upper and middle rectum is into the inferior mesenteric lymph nodes. Lymphatics in the lower rectum drain both superiorly into the inferior mesenteric lymph nodes and laterally into the internal iliac lymph nodes. Lymphatics from the anal canal proximal to the dentate line drain to both the inferior mesenteric lymph nodes and laterally to the internal iliac lymph nodes. Distal to the dentate line, lymph primarily drains into the inguinal nodes, but can also drain into the inferior mesenteric lymph nodes and internal iliac lymph nodes.17,20
Two distinct nervous compartments are found in the lower pelvis separated by the levator ani muscle (Fig. 1.2). In the infralevatory pathway, the pudendal nerve arises from the sacral plexus and runs via the ischioanal fossa to the genitals. The supralevatory pathway comprises both the superior hypogastric plexus as a network of sympathetic fibers situated just below the aortic bifurcation and the pelvic splanchnic nerves. The former is above continuous with the inferior mesenteric plexus and caudally fibers exit as the hypogastric nerves, which unite the superior and inferior hypogastric pelvic plexuses.2225
The hypogastric nerve descends into the pelvic cavity parallel to the ureter and internal iliac artery along the pelvic side wall (Fig. 1.3). The hypogastric nerves are usually more adherent to the visceral fascia covering the mesorectum than the pelvic sidewall and lie anterior to the retrorectal space.
The hypogastric nerve forms the inferior hypogastric or pelvic plexus at the lateral pelvic sidewall by encountering the parasympathetic sacral nerves (nervi erigentes or splanchnic nerves) originating from the 2nd, 3rd and 4th sacral roots.23287
zoom view
Figure. 1.2: Nerve supply to the rectum and anal canal103
zoom view
Figure. 1.3: Anatomic dissection
This plexus is sometimes revealed 8as a matted rhomboid structure with dimensions of 4 cm by 2.5 cm, lying almost in the sagittal plane lateral to the rectum.28, 29 The distance between the lateral rectum and the pelvic plexus is only 2–3 mm.30 There are abundant left/right communicating nerves between bilateral pelvic plexuses in front of Denonvilliers' fascia.31 In the male, a useful marker for its midpoint is the tip of the seminal vesicle. Laterally, it is tethered within the fascia on the sidewall of the pelvis. Medially, it is tethered by its branches.
The lateral ligaments of the rectum have long been the subject of anatomical confusion and surgical misconception.2527, 32, 33 A recent study locates it between rectum and visceral fascia within the mesorectum (Fig. 1.4).32 It is a pathway for the middle rectal arteries, the rectal branches from the pelvic plexus, and lymphatic vessels. The caudal margin of the lateral ligament has a close topographic relation with both the splanchnic nerves and the urogenital neurovascular bundle of Walsh.24, 27, 34, 35
The urogenital neurovascular bundle runs from its origin in the most posterior and caudal part of the inferior hypogastric plexus caudally of the lateral ligament in the groove between rectum and prostate to the periprostatic and perivesical plexuses. Parts of this bundle perforate the pelvic floor as cavernous nerve running into the cavernous body.24, 25
Although the levator ani muscle separates the two nervous compartments, there is still controversy about the innervation of this muscle. Several studies report no contribution of the pudendal nerve to the levator ani muscle but emphasize the existence of the levator ani nerve as a separate nerve branching directly from the sacral plexus to the levator ani muscle.3642
zoom view
Figure. 1.4: Schematic drawing of the lateral ligament of the rectum in total mesorectal excision
This nerve, which arises from sacral nerve roots S3–S5, is mentioned in various anatomy textbooks43, 44 but is still not clearly illustrated in others.45, 46
This theory is in contrast with several cadaver studies which report contributions of branches of the pudendal nerve to the innervation of the levator ani muscle.4750 A recent study in human fetuses confirms that the levator ani muscle has a dual somatic innervation but the contribution of the levator ani nerve to the innervation of the levator ani muscle is greater than that of the pudendal nerve. The contributions from the pudendal nerves are variable in both individuals and between both sides of the pelvis. Furthermore, a communicating branch between the levator ani nerve and the pudendal nerve is found in 56% of the specimens.51 Despite these findings, a recent study shows dual levator ani muscle innervation in 58.8% of cases and demonstrates exclusive levator ani muscle innervation from the pudendal nerve or levator ani nerve in 23.5% and 5.9% of cases, respectively. Finally, this study describes that individual muscle components of the levator ani muscle receive different contributions from the pudendal nerve or the levator ani nerve.47
The levator ani nerve approaches the levator ani muscle from within the pelvis on the superior surface of the pelvic floor, which could contribute to an increased risk of urinary and fecal incontinence after total mesorectal excision (TME).40, 41, 52, 53 In contrast, the pudendal nerve has only a minor contribution to the levator ani muscle innervation and runs inferior to the pelvic floor muscles and divides into the inferior rectal nerve, which innervates the external anal sphincter muscle and perineal skin; the perineal nerve which innervates the external anal sphincter and perineal muscles and the dorsal nerve of the clitoris/penis.47, 5051
Here, we discuss some key maneuvers allowing correct surgical oncology practice and prevent nerve injury.
Ligation of the IMA
Interruption of the blood supply during colorectal surgery can either be performed at the origin of IMA near the abdominal aorta, defined as high-tie ligation, or at the level of the SRA, defined as low-tie ligation (Fig. 1.5). Although no consensus exists on high-tie ligation of the IMA for oncological reasons, it is a common practice in rectal cancer surgery since high ligation avoids excessive traction in the anastomosis.5457 Several drawbacks should be kept in mind, however. At first, the risk of damage to the inferior mesenteric plexus which forms a dense network around the IMA is unavoidable in most cases.6, 2427, 30 Secondly, as stated above, this technique comprises the vascular supply to the distal transverse colon and left colon being dependent of the middle colic and marginal artery.6,1810
zoom view
Figure. 1.5: Point of division of the IMA during resection for rectosigmoid carcinomas: (A) High-tie ligation of the IMA involves division of the IMA at its origin from the aorta, (B) Low-tie ligation of the IMA preserves the left colic artery
Finally, high-tie ligation requires extended resection and mobilisation of the colon.6 Moreover, investigators recently demonstrated in formalin-fixed specimens, that it is not necessary to perform high-tie ligation in order to create a tension-free anastomosis. Low-tie ligation is applicable in 80% of cases.58 Some authors suggest to perform either high-tie or low-tie ligation based on the particular findings in each patient. Without clear advantages regarding long-term results, high-tie ligation should be avoided whenever possible in older or poor-risk patients.6
Total Mesorectal Excision
Recognition of the optimal surgical planes, preservation of the anatomy of the mesorectum, and sparing of the pelvic nerves are essential to perform a TME in a correct way enabling both total tumor excision and nerve-preserving surgery.24 When preservation of the autonomic nervous system was integrated into the therapeutic scheme for treatment of rectal cancer, the incidence of postoperative sexual and urinary complications has decreased to the range of 10%–35%, and <5%.59 Table 1.1 shows several dysfunctions due to injury to pelvic nerves.51, 6063
The rectum is surrounded by a layer of connective tissue and fat that contains the descending branches of the SRA, corresponding venous tributaries, autonomic nerves, and draining lymphatics and nodes. This layer is referred to as the mesorectum and is enclosed by the mesorectal fascia, also defined as the proper rectal fascia. The mesorectum is bulkier posteriorly and is of variable thickness.5, 23, 33, 64, 6511
Table 1.1   Dysfunctions due to injuries to autonomic pelvic nerves and levator ani nerve
Surgical nerve damage
Site of nerve damage
Bladder disorder
Male genital disorder
Female genital disorder
Anal sphincter disorder
Superior hypogastric plexus
Presacral mesorectal manipulation
Urgency and incontinence
Absent, retrograde or painful ejaculation
Diminished orgasm
Hypogastric nerve one side
Presacral mesorectal manipulation
Absent, retrograde or painful ejaculation
Hypogastric nerve both sides
Presacral mesorectal manipulation
Urgency and incontinence
Absent, retrograde or painful ejaculation
Diminished orgasm
Pelvic splanchnic nerve
Wide radical dissection
Voiding disorder
Erectile dysfunction
Reduced labial swelling
Inferior hypogastric plexus one side
S + P
Lateral ligament of the rectum or lateral mesorectal manipulation
Voiding disorder
Diminished erection + ejaculation
Incomplete vaginal lubrication/erection
Inferior hypogastric plexus both sides
S + P
Lateral ligament of the rectum or lateral mesorectal manipulation
Lack of erection + ejaculation
Lack of vaginal lubrication/erection
Neurovascular bundle one side
S + P
Dorsolateral to the prostate or lateral to the vagina
Diminished erection + ejaculation
Incomplete vaginal lubrication/erection; dyspareunia and impaired ability to reach orgasm
Neurovascular bundle both sides
S + P
Dorsolateral to the prostate or lateral to the vagina
Lack of erection + ejaculation
Lack of vaginal lubrication/erection; dyspareunia and impaired ability to reach orgasm
Levator ani nerve
Somatic innervation of LAM (S3–S5)
Visceral surface of LAM
S: sympathetic; P: parasympathetic; LAM: levator ani muscle
The concept of TME was first promoted by Heald in 1979.66 Essentially, the rationale for TME is based on the observation in pathology specimens that the mesorectum may harbor tumor deposits upto 4 cm distally from the lower border of the luminal tumor, whereas the macroscopic lower border of the luminal tumor usually corresponds with the microscopic margin. This finding has lead to the concept of removing the entire mesorectum in mid and lower rectal cancers. A second aspect of TME is sharp dissection of the rectum and its perirectal fat enclosed by the proper rectal fascia (circumferential resection margin) as one intact unit.23, 27, 6771 The current (2011) National Comprehensive Cancer Network guidelines recommend a circumferential resection margin of more than 1 mm. They emphasize incorporating distal margins which should be 4–5 cm for an adequate mesorectal excision. In distal rectal cancers, negative distal bowel wall margin of 1–2 cm may be acceptable.72 Preoperative MRI allows to define with great accuracy the relation between the tumor and the circumferential resection margin.73
The TME procedure results in improved survival (from 48%–>60%), reduced local recurrence rates (from >20% – <10%), and higher incidence of sphincter preservation.7413
At the beginning of the TME procedure, gentle anterior traction on the rectum and careful sharp dissection under direct vision reveals the retrorectal space situated between the mesorectal fascia and the parietal pelvic or presacral fascia (Figs 1.4 and 1.6). This relatively avascular areolar tissue plane or holy plane starts at the level of the promontory and extends in all directions and enables identification and preservation of the autonomic nerve plexus. As the dissection continues downward exposure gets poor in this plane.2, 23, 28, 69, 75, 76 Injury to the presacral fascia must be avoided. Entering the presacral space may result in purely sympathetic nerve damage and bleeding from the presacral veins.26, 27, 33
During the anterior dissection, the peritoneal reflection between the anterior wall of the rectum and the lower uterus or bladder is incised. Dissection is continued on the seminal vesicles or posterior vaginal wall.23 The appearance of Denonvilliers' fascia at operation varies considerably.26, 27 It is related to the prostate and seminal vesicles anteriorly, and to the rectal wall, the thin anterior mesorectum, and the fascia propria posteriorly.15, 26, 70 There is no longer evidence for two layers of Denonvilliers' fascia.24, 7779 Lateral to the seminal vesicles, the Denonvilliers' fascia consistently divides into multiple laminae.31
zoom view
Figure. 1.6: Retrorectal space
The dorsal-most lateral continuation of the Denonvilliers' fascia runs between the inferior hypogastric plexus and the mesorectum. During anterolateral rectal dissection in front of Denonvilliers' fascia the parasympathetic cavernous nerves originating periprostatically and piercing the pelvic floor are at risk for damage resulting in erectile dysfunction.24, 26, 27, 34, 80 As described above, the left/right communicating nerves between bilateral pelvic plexuses in front of the fascia and their lateral continuation are likely to be injured during surgery. These communications are also likely to compensate for functional losses in case of unilateral nerve injury.
Based on these results some authors propose to operate behind Denonvilliers' fascia.31 Other authors state that if the tumor is on the anterior wall of the rectum the plane of dissection happens between Denonvilliers' fascia and either the vagina or seminal vesicles/prostate gland, while on the posterior wall the dissection must be performed in the plane between the anterior rectal wall and Denonvilliers' fascia.76 However, Heald points out that the plane of dissection must be in front of Denonvilliers' fascia by making a U-shaped incision through this fascia to avoid damage to the anterolaterallying neurovascular bundles. In this way, Denonvilliers' fascia is retained to the specimen without compromising the oncologic outcome of the surgery.80
During TME it is frequently necessary to shift the focus of dissection.23 Inferiorly, the retrorectal space is crossed by the rectosacral fascia also known as Waldeyer's fascia, which firmly fuses with the mesorectal fascia approximately 3–5 cm proximal to the anorectal junction.5, 23, 27, 33 This fascia is considered as the junction between the free and fused parts of the presacral fascia. Cutting the rectosacral fascia and opening the retrorectal space laterally reveals the nervi erigentes.25 Failure to recognize and divide Waldeyer's fascia may result in either perforation of the rectum or hemorrhage from the presacral venous plexus. Thus, sharp division of the rectosacral fascia ensures an intact mesorectum. Full mobilization of the rectum is not possible unless the rectosacral fascia is divided. After division of the rectosacral fascia, the pelvic dissection goes down to the coccyx level.27, 28
The retrorectal space is minimal laterally where the inferior hypogastric plexus lies directly adhered to the mesorectal fascia.4, 25 The rectal branches arising from the pelvic plexus proceed along the lateral ligament of the rectum after passing its mesorectal fascia. This means that a correct execution of the TME in the plane between the visceral and parietal fascia does not reveal the lateral ligament.32 Straying laterally out of the mesorectal plane may injure the pelvic plexus if excess traction is placed on the rectum.23, 2527 Therefore, meticulous dissection should be performed on the fascia surrounding the mesorectum resulting in a careful separation of the pelvic plexus. Extracare at the converging 15lateral edges of Denonvilliers' fascia can avert damage to the hypogastric plexus.80 It is important to avoid mass ligation. If a MRA is encountered, it is recommended to ligate it with a surgical clip. The pattern of nerve damage here and beyond the pelvic plexus tends to be mixed sympathetic and parasympathetic. Authors suggest that in case of tumoral invasion of the rectal wall in middle or lower rectal cancer the pelvic plexus should be sacrificed.27 Radical lymphadenectomy procedures, as practised in Japan, may also lead to nerve injury in this zone and are not recommended.26
Continuation of the dissection posteriorly and laterally opens the plane between the mesorectum and coccygeal muscle and levator ani muscle. In the case of a low anterior resection, this plane will be dissected until the distal rectum is reached just above the anus. The perimesorectal dissection ends in an intersphincteric plane when the mesorectum tapers to an end.4,12, 23 In the case of a low anterior resection the rectum may be divided at this level.23 As stated above, the en bloc resection should have proximal, distal, and circumferential negative margins.81, 82
Advances in the fields of rectal surgery contribute to improved oncologic outcomes and result in more favorable functional results with a greater proportion of patients undergoing sphincter-preserving operations.83
Recent research shows clearness about certain topics in rectal cancer surgery while others are still not clarified. A review of the current literature is presented below.
It is generally accepted that high-volume surgeons specialized in colorectal surgery yield improved outcomes for patients with rectal cancer.84, 85
No consensus exist on high-tie ligation of the IMA for oncologic reasons. It is suggested to perform either high-tie or low-tie ligation based on the particular findings in the individual patient.5457 Correct surgical oncology practice means adequate inferior mesenteric lymphadenectomy and resection of the mesorectum as one intact unit (TME) with circumferential and distal margins of more than 1 mm and 4–5 cm, respectively. In distal rectal cancers, sphincter-saving surgery is acceptable if negative distal bowel wall margins of 1–2 cm are feasible.72 When respecting these rules, correct execution of the TME is associated with a reduced risk of local recurrence. Abdominoperineal resection is a valuable alternative for very low tumors.86
According to the guidelines from the International Union Against Cancer (UICC)/American Joint Committee on Cancer (AJCC) at least twelve lymph nodes should be taken and analyzed to allow appropriate nodal staging in both stage II and stage III colorectal cancer (CRC). Recently, it has been demonstrated that the lymph node ratio, defined as the ratio of the number of positive nodes over the total number of 16examined nodes, has superior prognostic stratification compared to the number of positive lymph nodes in stage III CRC.87 Currently, there is no general agreement concerning the preferred LNR cut-off value that allows optimal separation of subgroups of stage III patients.8790
In patients with early rectal cancer, the choice of treatment is complete local excision or TME, and depends on the risk of lymph node involvement, which is associated with the depth of invasion of the tumor in the rectal wall. Local excision-transanal excision or endoscopic microsurgery for tumors in the upper-third layer of the submucosa (T1Sm1) and some in the middle layer (T1Sm2) is valuable if excision is completed with adequate margins.86 Rectal tumors showing an excellent response to chemoradiotherapy may be suitable for local excision, with equivalent outcomes to radical surgery. This approach should be the subject of prospective clinical trials in specialist centers.91
The CLASICC trial, comparing laparoscopically assisted and open surgery for colorectal cancer in terms of overall survival, disease-free survival, and local and distal recurrence shows no differences after 5 year follow-up. But overall survival for patients who had conversion to open surgery is significantly worse and independent of a surgeon-related factor. Whether a high vascular ligation and complete regional lymphadenectomy can be achieved by laparoscopic means, and whether it is justified in all cases, remains to be determined.92 Although cancer related outcomes are hopeful, there is currently no evidence that laparoscopic TME preserves urogenital function more effectively than the open approach.74 Moreover, the early results of the CLASICC study showed no adverse effects on bladder function but a trend towards worse male sexual function after laparoscopic surgery.93 The results of other multicenter randomized controlled trials as the COLOR II, Japanese JCOG 0404, and ACOSOG Z6051 trials are awaited.9496
Anastomotic leakage is a severe complication after rectal cancer surgery. The relationship between anastomotic leakage and oncologic results is still controversial.97, 98 The leak rate varies considerably among clinical trials from 3% upto 23% in part owing to the lack of a standarized definition. A consensus definition and severity grading of this complication is recently developed within the International Study Group of Rectal Cancer and proposed to apply in future clinical reports. Leakage is considered as a defect of the intestinal wall at the anastomotic site leading to a communication between the intra and extraluminal compartments. Grade A anastomotic leakage results in no change in patients' management, whereas grade B leakage requires active therapeutic intervention but is manageable without relaparotomy. Grade C anastomotic leakage requires relaparotomy.83
A review of pouch reconstructions for rectal cancer shows a lower incidence of anastomotic leaks (<5%) using a colonic J-pouch of 5 cm derived from the sigmoid colon. One reason for the difference in the 17leakage rate may be that the microcirculation at the apex of the pouch is better preserved in comparison to the bowel end in the straight reconstruction.99
Although limited by the low methodological quality of the included trials, a Cochrane review concludes that covering ileo- or colostomy seems to be useful to prevent anastomotic leakage and urgent reoperations in patients receiving low anterior resection for rectal cancer. However, covering stoma does not offer advantage in term of 30 days or long term mortality.100 Even though authors endorse ileostomy over colostomy, controlled trials are needed to clarify which is the preferred technique.101
As stated above, anterior resection with preservation of the sphincter function has become the preferred treatment for rectal cancer, except for those cancers very close to the anal sphincter. An important reason for this has been the conviction that the quality of life for patients with a colostomy after abdominoperineal excision was poorer than for patients undergoing an operation with a sphincter-preserving technique. A Cochrane study which intended to compare the quality of life in rectal cancer patients with or without permanent colostomy could not meta-analysis the included studies due to heterogeneity and the fact that all included studies were observational trials. Larger and better designed studies are needed.102
Patients having sphincter-preserving operations may experience symptoms affecting their quality of life that are different from stoma-patients. A review of colonic J-pouch reconstruction shows superior functional outcome even 2 years or more after surgery in patients whose anastomosis is less than 8 cm from the anal verge. Patients with ultralow anastomoses, less than 4 cm from the anal verge, appear to benefit the most.99
Anatomic research shows a major contribution of the levator ani nerve to the innervation of the levator ani muscle. Due to its course on the superior surface of the pelvic floor, this nerve can be damaged during TME causing urinary and fecal incontinence.40, 41, 52, 53
In the light of a recent study, the course of the lateral ligament at the level of the lower rectum is better understood. It runs laterally within the mesorectum from the visceral fascia to the rectum, making it impossible to encounter during correct TME.32
  1. Martini FH, Timmons MJ, Tallitsch RB. Human Anatomy. The digestive system. Benjamin-Cummings Publishing Company.  San Francisico:  2004; 663–702.
  1. Godlewski G, Prudhomme M. Embryology and anatomy of the anorectum. Basis of surgery. Surg Clin North Am 2000; 80 (1): 319–43.
  1. Kluth D. Embryology of anorectal malformations. Semin Pediatr Surg 2010; 19 (3): 201–8. 18
  1. Mortenson M, Khatri VP, Bennett JJ, Petrelli NJ. Total mesorectal excision and pelvic node dissection for rectal cancer: An appraisal. Surg Oncol Clin N Am 2007; 16 (1): 177–97.
  1. Salerno G, Sinnatamby C, Branagan G, Daniels IR, Heald RJ, Moran BJ. Defining the rectum: Surgically, radiologically and anatomically. Colorectal Dis 2006; 8 Suppl 3: 5–9.
  1. Sakorafas GH, Zouros E, Peros G. Applied vascular anatomy of the colon and rectum: Clinical implications for the surgical oncologist. Surg Oncol 2006; 15 (4): 243–55.
  1. Rosenblum JD, Boyle CM, Schwartz LB. The mesenteric circulation: Anatomy and physiology. Surg Clin North Am 1997; 77 (2): 289–306.
  1. Lin PH, Chaikof EL. Embryology, anatomy, and surgical exposure of the great abdominal vessels. Surg Clin North Am. 2000 Feb; 80 (1): 417–33.
  1. Moskowitz M, Zimmerman H, Felson B. The meandering mesenteric artery of the colon. Am J Roentgenol Radium Ther Nucl Med 1964; 92: 1088–99.
  1. Sagar PM, Pemberton JH (Eds). Topographic anatomy. Surgery of the colon and rectum. Churchill Livingstone.  Philadelphia,  1997; 1–18.
  1. Drummond H: The arterial supply of the rectum and pelvic colon. Br J Surg 1913; 1: 677–82.
  1. Allison AS, Bloor C, Faux W, et al. The angiographic anatomy of the small arteries and their collaterals in colorectal resections: Some insights into anastomotic perfusion. Ann Surg 2010; 251 (6): 1092–7.
  1. Sato K, Sato T. The vascular and neuronal composition of the lateral ligament of the rectum and the rectosacral fascia. Surg Radiol Anat 1991; 13 (1): 17–22.
  1. DiDio LJ, Diaz-Franco C, Schemainda R, Bezerra AJ. Morphology of the middle rectal arteries. A study of 30 cadaveric dissections. Surg Radiol Anat 1986; 8 (4): 229–36.
  1. Nano M, Levi AC, Borghi F, et al. Observations on surgical anatomy for rectal cancer surgery. Hepatogastroenterology 1998; 45 (21): 717–26.
  1. Jones OM, Smeulders N, Wiseman O, et al. Lateral ligaments of the rectum: An anatomical study. Br J Surg 1999; 86 (4): 487–9.
  1. Brunicardi FC, Andersen DK, Billiar TR, Dunn DL, Hunter JG, Pollock RE. Colon, Rectum, and Anus. Schwartz's Principles of Surgery. McGraw-Hill Professional.  New York:  2005, 1055–118.
  1. Dworkin MJ, Allen-Mersh TG. Effect of inferior mesenteric artery ligation on blood flow in the marginal artery-dependent sigmoid colon. J Am Coll Surg 1996; 183 (4): 357–60.
  1. Douard R, Chevalier JM, Delmas V, Cugnenc PH. Clinical interest of digestive arterial trunk anastomoses. Surg Radiol Anat 2006; 28 (3): 219–27.
  1. Doherty GM, Way LW. Anorectum. Current surgical diagnosis and treatment. McGraw-Hill Professional.  New York:  2006; 764.
  1. Galandiuk S, Chaturvedi K, Topor B. Rectal cancer: A compartmental disease. The mesorectum and mesorectal lymph nodes. Recent Recults Cancer Res 2005; 165: 21–9.
  1. Bharucha AE. Pelvic floor: Anatomy and function. Neurogastroenterol Motil 2006; (18): 507–19.
  1. Havenga K, Grossmann I, DeRuiter M, Wiggers T. Definition of total mesorectal excision including the perineal phase: Technical considerations. Dig Dis 2007; 25: 44–50.
  1. Clausen N, Wolloscheck T, Konerding MA. How to optimize autonomic nerve preservation in total mesorectal excision: Clinical topography and morphology of pelvic nerves and fasciae. World J Surg 2008; 32: 1768–75.
  1. Kirkham AP, Mundy AR, Heald RJ, Scholefield JH. Cadaveric dissection for the rectal surgeon. Ann R Coll Surg Engl 2001; 83: 89–95. 19
  1. Lindsey I, Guy RJ, Warren BF, Mortensen NJ. Anatomy of Denonvilliers' fascia and pelvic nerves, impotence, and implications for the colorectal surgeon. Br J Surg 2000; 87 (10): 1288–99.
  1. Kim NK. Anatomic basis of sharp pelvic dissection for curative resection of rectal cancer. Yonsei Medical J 2005; 46: 737–49.
  1. Havenga K, DeRuiter MC, Enker WE, Welvaart K. Anatomical basis of autonomic nerve-preserving total mesorectal excision for rectal cancer. Br J Surg 1996; 83: 384–8.
  1. Havenga K, Maas CP, DeRuiter MC, Welvaart K, Trimbos JB. Avoiding long-term disturbance to bladder and sexual function in pelvic surgery, particularly with rectal cancer. Semin Surg Oncol 2000; 18 (3): 235–43.
  1. Höer J, Roegels A, Prescher A, Klosterhalfen B, Töns C, Schumpelick V. Preserving autonomic nerves in rectal surgery. Results of surgical preparation on human cadavers with fixed pelvic sections. Chirurg 2000; 71 (10): 1222–9.
  1. Kinugasa Y, Murakami G, Uchimoto K, Takenaka A, Yajima T, Sugihara K. Operating behind Denonvilliers' fascia for reliable preservation of urogenital autonomic nerves in total mesorectal excision: A histologic study using cadaveric specimens, including a surgical experiment using fresh cadaveric models. Dis Colon Rectum 2006; 49 (7): 1024–32.
  1. Lin M, Chen W, Huang L, Ni J, Yin L. The anatomy of lateral ligament of the rectum and its role in total mesorectal excision. World J Surg 2010 Mar; 34 (3): 594–8.
  1. Zhang C, Ding ZH, Li GX, Yu J, Wang YN, Hu YF. Perirectal fascia and spaces: Annular distribution pattern around the mesorectum. Dis Colon Rectum 2010; 53 (9): 1315–22.
  1. Wang GJ, Gao CF, Wei D, Wang C, Meng WJ. Anatomy of the lateral ligaments of the rectum: A controversial point of view. World J Gastroenterol 2010; 16: 5411–15.
  1. Nano M, Dal Corso HM, Lanfranco G, Ferronato M, Hornung JP. Contribution to the surgical anatomy of the ligaments of the rectum. Dis Colon Rectum 2000; 43 (11): 1592–97.
  1. Matzel KE, Schmidt RA, Tanagho EA. Neuroanatomy of the striated muscular anal continence mechanism. Implications for the use of neurostimulation. Dis Colon Rectum 1990; 33 (8): 666–73.
  1. Snooks SJ, Swash M. The innervation of the muscles of continence. Ann R Coll Surg Engl 1986; 68 (1): 45–9.
  1. Madoff RD, Parker SC, Varma MG, et al: Faecal incontinence in adults. Lancet 2004; 364: 621–32.
  1. Percy JP, Neill ME, Swash M, Parks AG. Electrophysiological study of motor nerve supply of pelvic floor. Lancet 1981; 1: 16–7.
  1. Barber MD, Bremer RE, Thor KB, Dolber PC, Kuehl TJ, Coates KW. Innervation of the female levator ani muscles. Am J Obstet Gynecol 2002; 187: 64–71.
  1. Azpiroz F, Fernandez-Fraga X, Merletti R, Enck P. The puborectalis muscle. Neurogastroenterol Motil 2005; 17: 68–72.
  1. Shobeiri SA, Chesson RR, Gasser RF. The internal innervation and morphology of the human female levator ani muscle. Am J Obstet Gynecol 2008; 199 (6): 686.
  1. Netter FH. Atlas of Human Anatomy. Elsevier  Philadelphia:  2011.
  1. Drake RL, Vogl W, Mitchell AWM. Gray's Anatomy for Students. Elsevier  Philadelphia:  2010.
  1. Putz R, Pabst R. Sobotta Atlas of Human Anatomy. Urban and Fischer  Philadelphia:  2006.
  1. Marieb EN, Mallat J, Wilhelm PB. Human Anatomy. Benjamin Cummings Publishing Company  San Francisco:  2008. 20
  1. Grigorescu BA, Lazarou G, Olson TR, et al. Innervation of the levator ani muscles: Description of the nerve branches to the pubococcygeus, iliococcygeus, and puborectalis muscles. Int Urogynecol J Pelvic Floor Dysfunct 2008; (19) 1: 107–16.
  1. Shafik A, el-Sherif M, Youssef A, Olfat ES. Surgical anatomy of the pudendal nerve and its clinical implications. Clin Anat 1995; 8 (2): 110–5.
  1. Shafik A, Doss S. Surgical anatomy of the somatic terminal innervation to the anal and urethral sphincters: Role in anal and urethral surgery. J Urol 1999; 161 (1): 85–9.
  1. Schraffordt SE, Tjandra JJ, Eizenberg N, Dwyer PL. Anatomy of the pudendal nerve and its terminal branches: A cadaver study. ANZ J Surg 2004; 74: 23–6.
  1. Wallner C, van Wissen J, Maas CP, Dabhoiwala NF, DeRuiter MC, Lamers WH. The contribution of the levator ani nerve and the pudendal nerve to the innervation of the levator ani muscles: A study in human foetuses. Eur Urol 2008; 54 (5): 1136–44.
  1. Wallner C, Maas CP, Dabhoiwala NF, Lamers WH, DeRuiter MC. Innervation of the Pelvic Floor Muscles. A Reappraisal for the Levator Ani Nerve. Obstet Gynecol 2006; 108 (3pt 1) 529–34.
  1. Wallner C, Lange MM, Bonsing B, et al. Causes of fecal and urinary incontinence after total mesorectal excision for rectal cancer based on cadaveric surgery: A study from the cooperative clinical investigators of the dutch total mesorectal excision trial. J Clin Oncol 2008; 26 (27): 4466–72.
  1. Pezim ME, Nicholls RJ. Survival after high or low ligation of the inferior mesenteric artery during curative surgery for rectal cancer. Ann Surg 1984; 200 (6): 729–33.
  1. Surtees P, Ritchie JK, Phillips RK. High versus low ligation of the inferior mesenteric artery in rectal cancer. Br J Surg 1990; 77 (6): 618–21.
  1. Corder AP, Karanjia ND, Williams JD, Heald RJ. Flush aortic tie versus selective preservation of the ascending left colic artery in low anterior resection for rectal carcinoma. Br J Surg 1992; 79 (7): 680–2.
  1. Uehara K, Yamamoto S, Fujita S, Akasu T, Moriya Y. Impact of upward lymph node dissection on survival rates in advanced lower rectal carcinoma. Dig Surg 2007; 24 (5): 375–81.
  1. Buunen M, Lange MM, Ditzel M, Kleinrensink GJ, van de V elde CJ, Lange JF. Level of arterial ligation in total mesorectal excision (TME): An anatomical study. Int J Colorectal Dis 2009; 24 (11): 1317–20.
  1. Eveno C, Lamblin A, Mariette C, Pocard M. Sexual and urinary dysfunction after proctectomy for rectal cancer. J Visc Surg 2010 Feb; 147 (1): e21–30.
  1. Rees PM, Fowler CJ, Maas CP. Sexual function in men and women with neurological disorders. Lancet 2007 Feb 10;369 (9560): 512–25.
  1. Maas K, Moriya Y, Kenter G, Trimbos B, van de Velde C. A plea for preservation of the pelvic autonomic nerves. Lancet 1999 Aug 28; 354 (9180): 772–3.
  1. Moriya Y. Function preservation in rectal cancer surgery. Int J Clin Oncol 2006 Oct; 11 (5): 339–43.
  1. Moszkowicz C, Alsaid B, Bessede T, Penna C, Nordlinger B, Benoît G, Peschaud F. Where does pelvic nerve injury occur during rectal surgery for cancer? Colorectal Dis 2010 Aug 16.
  1. Heald RJ. The ‘Holy Plane’ of Rectal Surgery. J R Soc Med 1988; 81 (9): 503–8.
  1. Mirilas P, Skanalakis JE. Surgical anatomy of the retroperitoneal spaces part II: The architecture of the retroperitoneal space. Am Surg 2010; 76 (1): 33–42. 21
  1. Heald RJ: A new approach to rectal cancer. Br J Hosp Med 1979; 22: 277–81.
  1. Bisset IP, Chau KY, Hill GL. Extrafascial excision of the rectum: Surgical anatomy of the fascia propria. Dis Colon Rectum 2000; 43 (7): 903–10.
  1. Diop M, Paratte B, Tatu L, Vuillier F, Brunelle S, Monnier G. Mesorectum: The surgical value of an anatomical approach. Surg Radiol Anat 2003; 25 (3–4): 290–304.
  1. Heald RJ, Husband EM, Ryall RD: The mesorectum in rectal cancer surgery: The clue to pelvic recurrence? Br J Surg 1982; 69: 613–16.
  1. Heald RJ, Moran BJ. Embryology and anatomy of the rectum. Semin Surg Oncol 1998; 15 (2): 66–71.
  1. Göhl J, Hohenberger W, Merkel S. Lymph node dissection in rectal carcinoma: TME and what else? Onkologie 2009; 32 (1–2): 57–61.
  1. National Comprehensive Cancer Network (NCCN) Rectal Cancer Guidelines. Version 2. 2011.
  1. Mercury Study Group. Diagnostic accuracy of preoperative magnetic resonance imaging in predicting curative resection of rectal cancer: Prospective observational study. BMJ. 2006 14;333 (7572): 779.
  1. Lange MM, van de Velde CJ. Urinary and sexual dysfunction after rectal cancer treatment. Nat Rev Urol. 2011 Jan; 8 (1): 51–7.
  1. Lin MB, Jin ZM, Yin L, et al. Understanding the planes of total mesorectal excision through surgical anatomy of pelvic fascia. Zhonghua Wei Chang Wai Ke Za Zhi 2008; 11 (4): 308–11.
  1. Stewart DB, Dietz DW. Total mesorectal excision: What are we doing? Clin Colon Rectal Surg 2007; 20 (3): 190–202.
  1. Kourambas J, Angus DG, Hosking P, Chou ST. A histological study of Denonvilliers' fascia and its relationship to the neurovascular bundle. Br J Urol 1998; 82 (3): 408–10.
  1. Lepor H, Gregerman M, Crosby R, Mostofi FK, Walsh PC. Precise localization of the autonomic nerves from the pelvic plexus to the corpora cavernosa: A detailed anatomical study of the adult male pelvis. Urol 1985; 133 (2): 207–12.
  1. van Ophoven A, Roth S. The anatomy and embryological origins of the fascia of Denonvilliers: A medico-historical debate. J Urol 1997; 157 (1): 3–9.
  1. Heald RJ, Moran BJ, Brown G, Daniels IR. Optimal total mesorectal excision for rectal cancer is by dissection in front of Denonvilliers' fascia. Br J Surg 2004; 91: 121–3.
  1. Goldberg S, Klas JV. Total mesorectal excision in the treatment of rectal cancer: a view from the USA. Semin Surg Oncol 1998; 15 (2): 87–90.
  1. Birbeck KF, Macklin CP, Tiffin NJ, et al. Rates of circumferential resection margin involvement vary between surgeons and predicts outcome in rectal cancer surgery. Ann Surg 2002; 235 (4): 449–57.
  1. Rahbari NN, Weitz J, Hohenberger W, et al. Definition and grading of anastomotic leakage following anterior resection of the rectum: A proposal by the International Study Group of Rectal Cancer. Surg 2010 Mar; 147 (3): 339–51.
  1. Nugent E, Neary P. Rectal cancer surgery: Volume-outcome analysis. Int J Colorectal Dis 2010 Dec; 25 (12): 1389–96.
  1. Archampong D, Borowski DW, Dickinson HO. Impact of surgeon volume on outcomes of rectal cancer surgery: A systematic review and meta-analysis. Surgeon 2010 Dec; 8 (6): 341–52.
  1. Cunningham D, Atkin W, Lenz HJ, Lynch HT, Minsky B, Nordlinger B, Starling N. Colorectal cancer. Lancet 2010 Mar 20;375 (9719): 1030–47. 22
  1. Ceelen W, Van Nieuwenhove Y, Pattyn P. Prognostic value of the lymph node ratio in stage III colorectal cancer: A systematic review. Ann Surg Oncol 2010 Nov; 17 (11): 2847–55.
  1. Tong LL, Gao P, Wang ZN, Song YX, Xu YY, Sun Z, Xing CZ, Wang X, Xu HM. Can lymph node ratio take the place of pN categories in the UICC/AJCC TNM classification system for colorectal cancer? Ann Surg Oncol 2011; 18 (9): 2453–60.
  1. Qiu HB, Zhang LY, Li YF, Zhou ZW, Keshari RP, Xu RH. Ratio of metastatic to resected lymph nodes enhances to predict survival in patients with stage III colorectal cancer. Anal Surg Oncol 2011Jun; 18 (6): 1568–74.
  1. Mouq SJ, McColl G, Lloyd SM, Wilson G, Saldanha JD, Diament RH. Comparison of positive lymph node ratio with an inflammation-based prognostic score in colorectal cancer. Br J Surg 2011 Feb; 98 (2): 282–6.
  1. Smith FM, Waldron D, Winter DC. Rectum-conserving surgery in the era of chemoradiotherapy. Br J Surg 2010 Dec; 97 (12): 1752–64.
  1. Jayne DG, Thorpe HC, Copeland J, Quirke P, Brown JM, Guillou PJ. Five-year follow-up of the medical research council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg 2010 Nov; 97 (11): 1638–45.
  1. Jayne DG, Brown JM, Thorpe H, Walker J, Quirke P, Guillou PJ. Bladder and sexual function following resection for rectal cancer in a randomized clinical trial of laparoscopic versus open technique. Br J Surg 2005 Sep; 92 (9): 1124–32.
  1. Buunen M, Bonjer HJ, Hop WC. COLOR II. A randomized clinical trial comparing laparoscopic and open surgery for rectal cancer. Dan Med Bull. 2009; 56: 89–91.
  1. Kitano S, Inomata M, Sato A, Yoshimura K, Moriya Y. Japan Clinical Oncology Group Study. Randomized controlled trial to evaluate laparoscopic surgery for colorectal cancer: Japan Clinical Oncology Group Study Jpn J Clin Oncol 2005; 35 (8): 475–7.
  1. Fleshman J. American College of Surgeons Oncology Group (ACOSOG)- Z6051. A phase III prospective randomized trial comparing laparoscopic-assisted resection versus open resection for rectal cancer. .
  1. Mantzoros I. Oncologic impact of anastomotic leakage after low anterior resection for rectal cancer. Tech Coloproctol 2010 Nov;14 suppl 1: S39–41.
  1. Moran BJ. Predicting the risk and diminishing the consequences of anastomotic leakage after anterior resection for rectal cancer. Acta Chir Iugosl 2010; 57 (3): 47–50.
  1. Hida J, Okuno K. Pouch operation for rectal cancer. Surg Today 2010 Apr; 40 (4): 307–14.
  1. Montedori A, Cirocchi R, Farinella E, Sciannameo F, Abraha I. Covering ileo- or colostomy in anterior resection for rectal cancer. Cochrane Database Syst Rev 2010, Issue 5. Art. No.: CD006878.
  1. Rondelli F, Reboldi P, Rulli A, et al. Loop ileostomy versus loop colostomy for fecal diversion after colorectal or coloanal anastomosis: A meta-analysis. Int J Colorectal Dis 2009; 24: 479–88.
  1. Pachler J, Wille-Jorgenson P. Quality of life after rectal resection for cancer, with or without permanent colostomy. Cochrane Database Syst Rev 2005, Issue 2. Art. No.: CD004323.
  1. Dyck PJ. Thomas PK (Eds). Autonomic and somatic systems to the anorectum and pelvic floor. In: Peripheral neuropathy, 4th ed. Elsevier Saunders  Philadelphia:  PA: 2005; 37: 279–98.