Anatomy, Physiology, and Measurement of Physiologic Function for Colorectal Surgery

gastrointestinal tract and abdomen ANATOMY, PHYSIOLOGY, AND MEASUREMENT OF PHYSIOLOGIC FUNCTION FOR COLORECTAL SURGERY

M. Nicole Lamb, MD, and Andreas M. Kaiser, MD, FACS, FASCRS

Solid surgical decision making and operative planning are The inferior mesenteric artery (IMA) provides the blood the cornerstones of excellence in outcomes and performance. supply to the hindgut, which is the origin for the distal Beyond the knowledge of the pathologic process, they transverse colon, the descending and sigmoid colon, the require an in-depth understanding of the anatomy and rectum, and the proximal anus.4 The distal anus is derived physiology of the area impacted by disease or dysfunction. from ectoderm and receives its blood supply from the inter- The embryology and anatomy, as well as the physiology nal pudendal artery. The dentate line marks the divide of the appendix, colon, rectum, and anus, are reviewed between the endoderm-based hindgut and the ectodermal here, with a particular focus on their impact on surgical anal canal.4 Before the terminal end of the hindgut develops evaluation and decision making. into separate structures and ostia, its blind end forms a primitive cloaca, which is separated by the cloacal mem- Embryology brane from the ectodermal surface depression of the proctodeum.5 The cloaca gives rise to the urogenital and digestive The gastrointestinal tract embryologically is derived from system. The descent of the urorectal septum divides the the endoderm, which folds into a tubular structure and cloaca into the urogenital sinus and the anorectal pouch. differentiates into the foregut, midgut, and hindgut to form the respective epithelia and parenchymatous tissues of the Abnormalities in the development of the urorectal septum 5 visceral and thoracic organs. Their muscular and connective most commonly result in anorectal malformations (ARMs). tissue components are derived from the mesoderm. On both Seventy percent of ARMs are associated with congenital ends of the endoderm, fusion zones need to form to provide abnormalities of other organ systems. The most common the connection with the ectoderm. Located on its cephalad anomalies involve the urogenital system and spine/spinal oral end is the stomatodeum; on the caudad aboral end is cord.4,5 the proctodeum. The development of the embryonic midgut, hindgut, and Colon cloaca begins in the fourth week of gestation.1 Each of these embryologic structures is supplied by and grows around a general characteristics major vascular pedicle; these later become landmarks in the The colon measures approximately 150 cm in length.6 completed anatomy [see Table 1]. The defi nitive anatomy Length of instrument insertion during colonoscopy, how- evolves from axial growth (elongation), radial growth ever, is a rather unreliable parameter for orientation and for (budding of parenchymatous organs), rotation, and timely the same location may be quite different during insertion fusion. The genetic machinery, which is anything but understood in detail,2 enacts the construction blueprint with un- versus withdrawal; more defi nitive landmarks or tattooing paralleled precision. However, congenital abnormalities oc- are therefore necessary for correct identifi cation of a site of cur when some of these multiple steps fail to complete [see pathology prior to surgical resection. The colon diameter is Table 2]. very variable but generally largest at the cecum (6 to 8 cm) The epithelia of the small bowel, appendix, ascending and decreases along its course to the sigmoid colon (2.5 to colon, and the proximal two thirds of the transverse colon 4.0 cm).7,8 The smaller lumen in conjunction with the more are derived from the midgut. The vascular supply to the formed stool on the left side and an overall higher incidence midgut forms the superior mesenteric artery (SMA).3 In the of pathology (neoplasm, diverticulitis) are among the factors sixth week of gestation, the midgut temporarily herniates that conjoin to make the sigmoid a frequent point of large outside the abdominal cavity and rotates 270° in counter- bowel obstruction. Use of a narrow sigmoid for a coloanal clockwise direction around the SMA [see Figure 1]; later, in anastomosis lacks a suffi cient storage capacity and is associ- week 10, it returns to the abdominal cavity. ated with high-frequency bowel function (low anterior

Table 1 Artery-Dependent Embryologic Development of the Gastrointestinal System Embryologic Precursor Arterial Supply Developed Organs Foregut Celiac artery Esophagus to ligament of Treitz, including pancreas/liver Midgut Superior mesenteric artery Ligament of Treitz to proximal two thirds of transverse colon Hindgut Inferior mesenteric artery Distal third of transverse colon to proximal anus

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Table 2 Embryologic Development and Related Malformations Embryologic Step Normal Anatomy Malformation 270° counterclockwise rotation Transverse colon passing over root of Partial or complete malrotations small bowel Return of temporary herniation Intact abdominal wall Meckel diverticulum, omphalocele, urachal cyst Fusion of endoderm/cloacal membrane/ Formation of anus and urogenital Imperforate anus, congenital cloaca, congenital ectoderm system rectovaginal/urinary fistula Proximodistal migration of neural crest cells Autonomic innervation Hirschsprung disease

resection syndrome)9; creation of a lower pressure reservoir to 8 days, during which new cells are built at the base of the (e.g., by means of a colonic J pouch) has been advocated and crypt and migrate to the surface, where they are shed off. may prove benefi cial in the fi rst 12 to 24 months.10 Under healthy circumstances, the interstitium between the The colonic wall consists of fi ve layers: mucosa, submu- crypts is very thin and contains only a limited number of cosa, muscularis propria, adventitia, and serosa. In a clinical cells, none of which should be polymorphonuclear white setting, the wall architecture is best visualized by means of blood cells. endorectal or endoscopic ultrasonography. Five separate Tenia coli, haustra, and appendices epiploicae are defi n- layers can be distinguished as concentric rings: interface/ ing characteristics of the colon. The outer longitudinal mus- contact zone (inner white), mucosa and muscularis mucosae cle is separated into three teniae coli that travel along the (inner black), submucosa (middle white), muscularis anterior wall of the entire colon. The teniae conjoin on the propria (outer black), and adventitia/fat (outer white) [see cecum at the appendiceal base and broaden and coalesce at Figure 2].11 The strongest layer is the submucosa, followed at the rectum.7,14 During a sigmoid resection for diverticulitis, a distance by the muscularis propria, both of which must be the convergence of the teniae signals the minimal distal included in any bowel anastomosis to provide adequate resection margin that should be obtained as otherwise there strength.12 The depth of tumor invasion into the bowel wall is a much higher risk of recurrent attacks.11 is the basis for the T stage and an integral part of colon can- The colonic haustra are functional segmentations of the cer staging according to the TNM system by the American colon that result in its characteristic sacculated gross appear- Joint Commission on Cancer (AJCC).13 In contrast to the ance. On radiologic imaging, this haustriation of the colon small bowel, the colorectal mucosa does not form any villi allows for distinction from the small bowel, which shows but consists of crypts that are lined up back to back and are plicae circulares and less of a diameter variation. It should covered by a single layer of cylindrical cells. Intertwined are be noted, however, that disuse colitis or “burned-out” ulcer- mucus-producing goblet cells that increase in number ative colitis characteristically result in a loss of haustra (lead toward the rectum. There is a natural cell turnover within 4 pipe appearance).15

Figure 1 Malrotation syndrome (on small bowel follow-through with barium contrast). Figure 2 Colon/rectal wall layers on ultrasound.

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The external colon surface has varying degrees of appendices epiploicae, which are serosa-covered pedunculated fat pads; they are most prevalent toward the left colon and more evident in the completely intraperitoneal colon segments (transverse and sigmoid colon) and refl ect the patient’s body and fat habitus. Infl ammation, torsion, or ischemia of these appendices (characteristically in middle- aged individuals) can occasionally result in epiploic appendagitis with sudden onset of diffuse or localized abdominal pain and among other differential diagnoses may mimic acute appendicitis or diverticulitis. On a computed tomographic (CT) scan, however, there is no or little colonic wall thickening but characteristically a paracolonic, rim- enhanced ovoid structure with paracolic fat stranding.16 The pathology is a self-limited process that usually resolves within 5 days and does not require any surgical intervention.16 clinical impact: assessment of colonic anatomy For many conditions, the exact confi guration of the colon has little clinical impact. Excessive tortuosity (dolichocolon) may be a challenge for a colonoscopy but otherwise does not represent a condition that per se would require any treatment. Colonoscopy with direct visualization of the mucosa as the most frequent source of pathology remains the evaluation of choice.17 However, before carrying out a surgical intervention, it is mandatory to know the exact location of a pathology, and it may be necessary to have an understanding of the colon confi guration (road map). If the location of a pathology cannot be seen on cross-sectional imaging because it is too small (e.g., a relatively small tumor), the tool to defi ne the location consists of endoscopic tattooing of the area. An effort should be made to inject the India ink transmurally such that it becomes visible on the serosal side during the surgery (which, in the case of laparoscopy, lacks Figure 3 Computed tomographic colonography. the tactile sensation). For gross anatomy, a single-column contrast enema is suffi cient but will not provide structural mucosal details. A well-done barium-air double-contrast enema or CT colonography can provide that detail [see to the right fl ank, suprapubic area, or right upper quadrant. Figure 3].18 Nowadays, the diagnosis of acute appendicitis relies on a combination of symptoms, clinical signs, and cross-sectional imaging (CT, magnetic resonance imaging [MRI], or ultraso- Appendix nography), which aim at identifying an increase in wall The appendix vermiformis, as the name suggests, is a thickness and/or diameter along with periappendiceal fat narrow, wormlike structure with all histologic layers of a stranding, possibly abscess formation.22 The gravid uterus bowel wall; the base of the appendix is located at the other- adds even more complexity as it elevates the cecum and wise blind apex of the cecum, where the colonic teniae join appendix out of the pelvis and hence causes a gradual shift to form a continuous longitudinal muscular layer.7 The aver- of abdominal pain into the right upper quadrant and fl ank age length of the appendix is 9 cm (2 to 20 cm), a diameter region while limiting the use of harmful radiation-based less than 6 mm, and wall thickness less than 3 mm.19,20 The diagnostics. location of the base of the appendix is fairly constant within Anatomic structures adjacent to the appendix include the the variability of the cecal position (which may change due mesoappendix with the appendicular artery (an end branch to its fl oppiness or due to gravidity); the site of the appendix of the ileocolic artery) and vein. The ligament (or fat pad) tip, however, varies considerably but seems not to have of Treves is a nearly bloodless peritoneal ileocecal fold that undergone any major reevaluation since 1933, when 67.5% extends on the antimesenteric side of the terminal ileum to were reported to be retrocecal, 31% descending pelvic, 1% the base of the appendix.23 Dissecting through this ligament preileal, and 0.5% retroileal.7,21 In the preimaging era, this allows bloodless access to the base of the appendix during inconsistency was a major challenge as it was associated appendectomy. with blurring of the classic symptoms of appendicitis (epi- The biological function of the appendix is not entirely gastric dull pain, migrating to and becoming more sharp in understood, but it contains gut-associated lymphoid tissue the right lower quadrant) toward atypical presentations, (GALT) and appears to participate in immune functions with pain locations ranging from the right lower quadrant of the colon.24 The lymphoid tissue aids in maturing B

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03/15 gastro anatomy, physiology, and measurement of physiologic function for colorectal surgery — 4 lymphocytes and produces IgA antibodies.20 The appendi- toward the scrotum; in females, the gonadal vessels defl ect ceal epithelium secretes 2 to 3 mL of luminal mucin per day. at the pelvic brim toward the ovaries. A critical structure More recently, it has been proposed that the appendix during the right colon mobilization—either as the traditiona l releases an extracellular matrix, “biofi lm,” made of secretory lateral-to-medial dissection moves toward the hepatic fl ex- IgA and mucin that could play an important role in the ure or as a landmark during the medial-to-lateral approach “microbial ecology” of the gut.19,25 The biofi lm supports the in laparoscopy—is the duodenum, which is located postero- growth of colonies of bacteria within the colon and serves as medial to the hepatic fl exure and is generally substantially a protective barrier to infection.24,25 The loss of the appendix more caudal than anticipated by many beginning laparosco- after an appendectomy has not been shown to have any pists: the structure deserves to be handled with gentleness negative immunologic repercussions, even though some and needs to be carefully defl ected from the mesocolon [see data suggest that appendectomy before reaching adulthood Table 3]. The inferior pole of the right kidney is also posi- may be associated with a reduced incidence of ulcerative tioned below the hepatic fl exure. Further medial retraction colitis.26–29 of the right colon would provide exposure to the inferior vena cava and the root of the mesentery, but that extent is Cecum not commonly necessary. The laparoscopic approach has taught us a lot about natural planes to be used for the The cecum is the fi rst part of the colon but, strictly speak- dissection. The medial-to-lateral approach takes advantage ing, not within the continuity of the fecal stream but rather of the lateral attachment as an inherent retraction tool and a side street in the form of a blind-end pocket downward gains access to the retroperitoneal side of the mesocolon from the ileocecal valve. For that reason, it is not uncommon by defl ecting the duodenum posteriorly.32 At the hepatic during colonoscopy to fi nd the cecum less well cleaned fl exure, the colon—supported by the hepatocolic ligament— out than the rest of the colon, an observation that in itself often tracks posteriorly before it turns medially. On mobiliz- can add to the orientation. The cecum is either partially or ing the hepatic fl exure, vigorous medial retraction of the completely peritonealized and measures approximately colon can result in bleeding, either from the hepatocolic 6 cm in length.7 With an average of up to 8 cm diameter, it ligament, the liver itself when there are adhesions between is the widest part of the colon and—following LaPlace’s law the liver capsule and the colon or its mesentery, or, of physics (tension = pressure × radius)—carries the highest most dangerously, from vein branches of the superior risk of a perforation during states of increased colonic mesenteric vein. distention (large bowel obstruction), particularly when the ileocecal valve is competent and hence creates a closed-loop obstruction.30 Clinically or on imaging, a dynamic of a rapid Transverse Colon progression of the bowel distention to a cecal diameter The transverse colon is one of two fully intraperitoneal greater than 10 cm correlates with the threat of a subsequent colon segments. It hangs like a suspension bridge from the perforation. Radiographic signs of structural bowel wall hepatic to the often higher splenic fl exure and measures impairment include the presence of pneumatosis coli, that is, approximately 45 cm in length.31 Posterior and medial to gas bubbles within the bowel wall. A cecal volvulus (either around its axis or as a volvulus en bascule by folding trans- the splenic fl exure are the pancreas and the duodenum [see versely) is particularly dangerous as the distention is further Table 3]. The pericolonic spaces (lesser sac) and ligaments aggravated by a strangulating component with ensuing seem to be confusing at fi rst but are easily understood if the ischemia. The management of a patient with a cecal volvu- embryologic development of the peritoneal surface is taken lus requires swift action to, most commonly, perform a sur- into consideration. After the peritoneal cavity initially surgical resection or, on rare occasions, to untwist the torsion rounds the various organs, the lesser sac forms and bulges and perform a cecopexy.11 between the stomach and the transverse colon to form the gastrocolic ligament and a four-layer “napkin” that hangs from the transverse colon and develops into the omentum. Ascending Colon The gastrocolic ligament transitions seamlessly to the The ascending colon extends from the ileocecal junction to greater omentum, where it is attached to the anterior wall of the hepatic fl exure and measures approximately 15 cm in the colon. Mobilization of the transverse colon can be carried length.31 It is a partially retroperitoneal structure whereby out either as omentum sparing or by including the omentum the lateral attachment to the abdominal wall and the perito- with the resection.11 For the former, the omentum is lifted neal refl ection are marked by the white line of Toldt, the toward the stomach and gently dissected off the anterior entry point to the avascular plane used to mobilize the colon wall; for the latter, the gastrocolic ligament is divided, right colon. and the omentum is left on the transverse colon. By raising During mobilization of the right-sided colon, several the whole transverse colon cephalad and following the structures are at risk for inadvertent injury. The right ureter transverse mesocolon, the ligament of Treitz can be found— travels in the retroperitoneum anterior to the oblique psoas a practical maneuver during laparoscopic gastric bypass muscle, crosses the iliac vessels just medial to the iliac bifur- surgeries. cation, and continues to the lateral pelvic sidewall before it reaches the bladder. The gonadal artery and vein come together at the midlevel of the ureter, where they cross it to Descending Colon subsequently travel laterally to it. In males, they target the The left colon mirrors the ascending colon as it again is a internal inguinal ring and conjoin with the vas deferens partially retroperitoneal structure of approximately 25 cm in

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Table 3 Principles and Critical Structures during Colorectal Mobilization/Resection Surgical Mobilization Target Landmarks Avoid/At Risk Right colon Ileocecal junction, ileocecal vascular Appendix, ileocecal pedicle, white line of Right ureter, duodenum, pedicle, right branch of middle Toldt, duodenum, gastrocolic ligament, gastroepiploic vessels, colic artery, right half of bifurcation of midcolic artery gallbladder/liver, right omentum kidney Transverse colon Both flexures (hepatic/splenic), Runoff from SMA, midcolic bifurcation, Duodenum, proximal midcolic artery, variable: splenocolic ligament jejunum, pancreas, SMA, omentum SMV, spleen, liver Descending colon Distal transverse colon, splenic White line of Toldt, splenocolic ligament, Pancreas, spleen, left kidney, flexure, descendosigmoid IMA, bifurcation into left colic and IMV junction, IMA vs. left colic artery, superior rectal artery, IMV (inferior left branch of midcolic artery, edge of pancreas) IMV, left half of omentum Sigmoid colon Descendosigmoid junction, upper White line of Toldt, splenocolic ligament, Left ureter, gonadal vessels, rectum, IMA vs. superior rectal IMA, bifurcation into left colic and iliac artery/vein, hypogas- artery, IMV superior rectal artery, IMV (inferior tric nerves, presacral fascia, edge of pancreas), presacral fascia, presacral veins, spleen hypogastric nerves Rectum Midsigmoid to pelvic floor, IMA, bifurcation into left colic and Left ureter, gonadal vessels, mesorectum, fascia propria superior rectal artery, IMV (inferior iliac artery/vein, presacral edge of pancreas), presacral fascia, fascia, presacral veins, Waldeyer fascia, hypogastric nerves, hypogastric nerves, nervi fascia propria, Denonvilliers fascia, erigentes seminal vesicles/prostate, uterus/ vagina Anus (abdomino- Same as rectum, pelvic floor Abdominal: same as for rectum, perineal: Same as for rectum, urethra perineal resection) including sphincters, possibly coccyx, ischial tuberosities, transverse posterior vaginal wall perinei muscle, Foley catheter

IMA = inferior mesenteric artery; IMV = inferior mesenteric vein; SMA = superior mesenteric artery; SMV = superior mesenteric vein.

length, extending from the splenic fl exure to the beginning That is not typically a problem as the gained mobility by far of the intraperitoneal sigmoid loop.8 The lateral peritoneal outweighs the limited loss of bowel length. refl ection is marked by the white line of Toldt. As previously mentioned for the right side, the mobilization of the Sigmoid Colon left colon is started by opening the serosa along this line to access the avascular embryologic plane and gently defl ect The sigmoid colon is again a fully intraperitoneal colon the colon medially. The left ureter lies posterior to the left segment with a free mesocolon. It connects the lower edge colon (but medial to the gonadal vessels), traveling toward of the descending colon with the proximal rectum. The sig- the bifurcation of the common iliac arteries [see Table 3]. If moid is the narrowest section of the colon with an average otherwise diffi cult to identify, for example, in the setting diameter of 2.5 cm. Its length varies considerably from 15 to of severe infl ammation or dense adhesions from previous 50 cm,31 which is also associated with a substantial variabil- surgery in that area, it is best found as it crosses the iliac ity of its location such that symptoms emanating from it vessel; when diffi culties are anticipated, placement of are not necessarily limited to the left lower quadrant. For ureteral stents may be benefi cial and help in reducing the example, sigmoid diverticulitis can present with right lower risk of iatrogenic ureteral injury and, should it nonetheless quadrant pain and may be mistaken for acute appendicitis occur, improved recognition.11 or a gynecologic pathology. A redundant sigmoid colon The dissection follows the avascular plane toward the with a narrow-based mesentery is at an increased risk for splenic fl exure, which is at a more acute angle, higher, and volvulizing around its vascular pedicle. The volvulus results more posteriorly located than the hepatic fl exure. Releasing in obstruction and strangulation with associated clinical the splenic fl exure may be needed as part of the resection or symptoms; the characteristic x-ray image shows a distended to provide additional length to reach the pelvis for a low loop pointing from the left lower to the right upper colorectal/coloanal anastomosis. Excessive traction can quadrant (coffee bean sign); the condition requires swift result in tears of the splenic capsule and parenchyma and intervention to untwist and decompress the bowel before trigger severe bleeding. The attachments of the splenocolic irreversible structural damage occurs and/or to perform ligament need to be carefully released by staying close to the the necessary resection immediately or during the same colon wall. To further augment the colon mobility, transsec- hospitalization. tion of the restraining vascular structures (inferior mesen- The higher stool consistency, in conjunction with and teric artery and vein) may be necessary but could result in a aggravated by a low-fi ber diet and constipation, seems to compromised perfusion of the most distal colon segment. be associated with muscular hypertrophy; the increased

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03/15 gastro anatomy, physiology, and measurement of physiologic function for colorectal surgery — 6 intraluminal pressure may promote the mucosa and submu- just come out: they turn and hence get struck in a direction cosa to herniate outwards at the sites where blood vessels different from the one needed for evacuation.37 penetrate the muscle layer. As a result, “false diverticula” From a surgical and disease behavior perspective, almost form (i.e., pockets that do not involve all layers of the bowel nothing in regard to rectal anatomy is as important as a thor- wall).33 The thin wall and the anatomic association with the ough understanding of the pelvic fascias, which represent passage of blood vessels explain the two clinical pathologies the anatomic landmarks of a correct surgical dissection.14,38 that may evolve from diverticula: diverticular bleeding and These planes of tense fi brous tissue delineate virtual pelvic (2) diverticulitis (acute, chronic). Acute diverticulitis devel- compartments such as the mesorectal envelope. The meso- ops from a micro- to a macroperforation, and the spectrum rectal envelope (fascia propria of the rectum) represents an of its severity from mild to life threatening appears to be important even though not impenetrable border for the determined by the effectiveness of surrounding structures spread of rectal neoplasms. Maintaining the integrity of this to conceal the damage.11,34 The chronic infl ammation of compartment during a total mesorectal excision (TME) sigmoid diverticula can lead to a strictured segment or has been shown to be the key element of improved surgical fi stula development to surrounding organs, such as the technique and outcome.39 Damage to the envelope destroys bladder, uterus, vagina, small bowel, or even skin. the compartmental integrity and allows cancer cells to either remain unexcised or contaminate the operative fi eld, thus increasing the risk of local recurrence.40 As stated by the Rectum College of American Pathologists, the pathologist plays an general characteristics essential role in assessing the gross appearance of a resection specimen with regard to the fascial integrity.41 The rectum is the last and partially extraperitoneal seg- The endopelvic fascia covers the entire pelvis and consists ment of the large intestine. The peritoneum covers the upper of a visceral and a parietal leaf,14 which are separated by third of the rectum on its anterior and lateral aspects and an avascular areolar space [see Figure 5]. On the posterior extends anteriorly to the middle third, whereas the lower aspect, the visceral fascia (fascia propria) lines the mesorec- third typically is completely extraperitoneal. The exact tum, which, on the resected specimen, should have a smooth, length of the rectum has been defi ned in a variety of ways.14 shiny, and symmetrical appearance with a bilobar fatty Obsolete (because too variable) defi nitions include the posi- convexity.42,43 The parietal layer of the endopelvic fascia tion of the peritoneal refl ection (which varies around the (presacral fascia) covers the sacrum, the midsacral artery individual rectum itself and, for example, in patients with (that has a posterior runoff at the aortic bifurcation), and the rectal prolapse, is typically very low at the pelvic fl oor) or presacral veins, which are a potential source of severe pelvic the level of the sacral promontory (which changes once the bleeding if the mobilization of the rectum is carried out too 14 rectum is mobilized). posteriorly.14,38 The two fascial layers fuse a few centimeters From a surgical perspective, there are only two acceptable above the coccyx and form Waldeyer fascia.14,44 Complete defi nitions. The best delineation between the sigmoid colon mobilization of the rectum to the level of the pelvic fl oor and the beginning of the rectum is the point where the three requires sharp division of Waldeyer fascia behind the 14 colonic teniae coalesce into one (rectum). Since this can rectum. On the anterior aspect, Denonvilliers fascia is the only be visualized intraoperatively and treatment decisions extraperitoneal connective tissue layer that begins at have to be made before surgery and are different for the peritoneal refl ection and separates the space anterior to rectal versus sigmoid/colon cancers, the rectum can also the rectum from the prostate/seminal vesicles or posterior be defi ned by length only [see Table 4]. Locally advanced vagina, respectively.14,36 Laterally, the rectum does not rectal cancers are commonly treated with neoadjuvant display such a clear layer of separation but is surrounded by chemoradiation as opposed to sigmoid and other colon connective and fat tissue containing hypogastric and pelvic cancers, which are treated by surgery fi rst. The National nerves as well as the hypogastric blood vessels arising Cancer Institute has therefore defi ned the rectum as the from the pelvic sidewalls. Even though it does not have the 12 to 15 cm from the anal verge as measured by a rigid histologic elements of a ligament, this tissue—particularly sigmoidoscopy.14,35 in older nomenclature—was referred to as the “lateral The rectum is not a straight tube, but, in a retrograde ligaments.”8,14 direction, starts with a posterior curve above the puborecta- Although the mesorectum in the upper and midlevel lis sling (anorectal angle), after which it follows the concave of the rectum has a substantial cross-sectional volume, it anterior surface of the sacrum toward the promontory, inter- narrows down in the distal third as it approaches the pelvic rupted in transverse direction by three functional folds fl oor. Within the parietal fascial envelope of the mesorectum (valves of Houston), before it angles sharply at the pelvic are terminal branches of the IMA and a limited number of entry (rectosigmoid angle).14,36 Awareness of these angula- lymph nodes36; under normal circumstances, these lymph tions [see Figure 4] is crucial not only for safe insertion of a nodes are less than 4 to 5 mm and cannot typically be rigid instrument (proctoscope or end-to-end anastomosis distinguished from the surrounding fat on cross-sectional [EEA] stapler) but also because they lend themselves to imaging (such as endorectal ultrasonography, MRI, or CT).36 sonographic artifacts (false positive pathology) on ultraso- Infl ammation and metastatic disease increase the size and nography when the folds are hit tangentially.11 Furthermore, echogenicity (water content) of the lymph nodes, which ren- the angulations above the typically tight pelvic fl oor provide ders them more detectable during the pretreatment staging an explanation as to why rectal foreign bodies get lost once for rectal cancer.11,45 Positron emission tomography (PET) their end goes beyond the anal canal and do not typically may detect increased activity in cell metabolism (uptake of

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Table 4 Clinical Impact of Anatomic Differences between Colon and Rectum Variable Colon Rectum Definition Proximal Ileocecal valve Tenia confluence or 15 cm from anal verge Distal Tenia confluence or 15 cm from anal verge Dentate line Gross anatomy Partially to completely intraperitoneal segments: Partially to completely extraperitoneal: T4 tumor → T4 tumor → perforation/peritoneal seeding invasion into other organs Blood supply Visceral arteries (SMA/IMA): ischemia possible Visceral arteries (SMA/IMA) + somatic arteries (internal iliac): ischemia rare Venous drainage Portal vein system, metastatic disease → liver Portal vein system + systemic circulation (via vena cava): metastatic disease → liver/lung Lymph nodes Preoperative: no impact Preoperative: neoadjuvant chemoradiation Postoperative: adjuvant chemotherapy Postoperative: adjuvant consolidation chemotherapy Lymph drainage Unidirectional: low risk of local recurrence Multidirectional: higher risk of local recurrence Envelope Mesocolon: embryogenetic planes Mesorectum + fascia propria: fascial planes Environment Variable target, adjacency to radiosensitive small Relatively stable position within pelvic structures: bowel: radiation only very rarely used radiation very common Proximity Retro-/intraperitoneal structures Pelvic floor/sphincter Low probability of temporary vs. permanent stoma Significant probability of temporary vs. permanent stoma

IMA = inferior mesenteric artery; SMA = superior mesenteric artery.

18F-fl uorodeoxyglucose [FDG]) but generally has a greater the local recurrence rate from 28% to 8%46,47 and in a similar impact on detecting distant metastatic disease than on or even better magnitude than what the Swedish Rectal assessment of the local disease. Cancer Trial was able to achieve with the addition of radia- Identifi cation of the correct fascial layers in the upper and tion (11% with radiation + surgery compared with 27% with midrectum and of Waldeyer and Denonvilliers fascia in the surgery alone).48–50 Furthermore, respecting the planes of lower portion is critical to performing a correct TME.43 This dissection minimizes the negative impact on the autonomic specimen-oriented technique involves sharp dissection of nerves as the hypogastric nerves are generally visible and the mesorectal envelope along the areolar tissue and under preserved on top of the presacral fascia, hence limiting the direct vision down to the pelvic fl oor, whereby the bilateral negative impact on sexual and bladder function.51 hypogastric nerves are gently defl ected from the fascia propria.46 The TME technique was perfected and promoted by Heald, who in 1979 referred to this avascular plane as the “Holy Plane of Rectal Surgery.”39 Without the addition of radiation, implementation of this technique alone decreased

Valves of Houston Fascia Propria of Rectum

Peritoneum Levator Mesorectum Ani Muscle

Waldeyer Fascia Columns of Internal Denonvilliers Morgagni Levator Sphincter Fascia Ani Muscle Anococcygeal Dentate External Ligament Line Sphincter Anoderm

Figure 4 Coronal view of the rectum. Figure 5 Lateral view of the rectum.

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03/15 gastro anatomy, physiology, and measurement of physiologic function for colorectal surgery — 8 clinical impact: assessment of fascial envelope variable strength: the arc of Riolan connects the superior and The circumferential radial margin has been recognized as inferior mesenteric arteries more centrally, whereas the 57 a key prognostic factor for local recurrence after treatment marginal artery runs close to the edge of the colon. Due to a relatively limited collateralization, watershed areas are for rectal cancer.52,53 Pelvic MRI has evolved as the imaging found at the interface of two major arterial supply areas and tool of choice for that purpose [see Figure 6],54 whereas are the characteristic locations for ischemic events: the most ultrasonography remains preferred for assessment of the T notorious is at the splenic fl exure: the Griffi th point, which level.55 None of the techniques (CT, MRI, ultrasonography, refl ects the watershed area between the SMA and the IMA, PET) has shown superiority in assessing nodal involvement. where the marginal artery of Drummond is small and fi ne PET scans are relevant for detection of distant metastases (or sometimes absent).11,57 It is important not to create a and differentiation between scar tissue and local recurrence. transverse colostomy at the splenic fl exure due to its tenuous blood supply. Of historical signifi cance, Sudeck Blood Vessels described a critical point (1906) at the rectosigmoid junction that would be prone to ischemia; however, in 1956, Griffi th general characteristics refuted this by showing that there are collaterals between 3 The blood supply to the colon originates entirely from the the two systems. visceral arteries (superior and inferior mesenteric arteries) The rectum receives a triple blood supply and hence is and drains into the portal vein system [see Figure 7]. In much less frequently affected by ischemia. The superior contrast, the rectum also has a substantial component of hemorrhoidal/rectal artery, a branch of the IMA, is the main arterial source to the rectum. The middle and inferior its blood supply from and to the somatic circulation. As hemorrhoidal/rectal arteries reach the distal rectum and mentioned in the embryology section, the right-sided colon anus. They both originate from the internal iliac artery, up to a watershed area near the splenic fl exure obtains its either directly (middle) or indirectly via the internal puden- arterial blood fl ow from the SMA. After the pancreaticoduo- dal artery that travels through the Alcock canal (inferior).14 denal branches, the next and second branch of the SMA is The venous map in the periphery follows the arterial the midcolic artery that supplies the transverse colon, that is, supply but centrally has a distinct difference as the visceral paradoxically a bowel segment distal to the more proximal- blood fl ow is redirected through the portal system to the ly situated small bowel and right-sided colon segments, liver. The course of the inferior mesenteric vein separates whose blood supplies branch off more distally from the from the IMA and drains into the splenic vein at the lower SMA. With considerable variability, the colonic branches of edge of the pancreas. The superior mesenteric vein conjoins the SMA include the ileocolic artery (including the appen- with the splenic vein to form the portal vein. The venous dicular artery), the right colic artery, and the previously drainage of the rectum follows both a visceral and a 56 mentioned middle colic artery. systemic pattern: the superior hemorrhoidal vein drains The IMA supplies the left-sided colon from the splenic into the inferior mesenteric vein, whereas the middle and fl exure watershed area to the rectum and a portion of the inferior hemorrhoidal veins drain through the internal iliac anus. The IMA splits into the left colic artery (supplying the vein into the inferior vena cava and systemic circulation.14 splenic fl exure and the left colon) and the superior hemorrhoidal/rectal artery to the rectosigmoid and proximal anus. clinical impact: assessment of vascularization The superior and inferior mesenteric artery systems Even though bleeding remains one of the core symptoms are connected through a limited number of collaterals of in colon and rectal pathology, direct assessment of the vascularization is only rarely necessary. The arterial side might become relevant in (1) massive lower gastrointestinal bleeding for diagnostic and therapeutic indications (e.g., embolization) or (2) to defi ne the perfusion anatomy either after a previous surgical intervention of uncertain details or (3) when chronic or intermittent visceral ischemia is suspected. The venous side, due to the wide collaterals, is rarely affected and only if there is a fairly central impairment of the blood return, for example, by portal vein or complete vena cava thrombosis. The assessment tools include interventional angiography (with potential embolization) or magnetic resonance angiography if the specifi cs of vascularization need to be addressed. For less detail, evaluation with routine CT scans with intra- venous contrast provides some information. Functional fl ow information can be obtained with duplex ultrasonography.

Lymph Nodes general characteristics Figure 6 Magnetic resonance image of the pelvis in a patient with Lymph drainage follows the vascular anatomy with locally advanced rectal cancer. associated lymph nodes. The lymphatic plexus begin in the

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Middle Colic Artery

Marginal Artery of Drummond

Superior Mesenteric Artery

Ileocolic Inferior Artery Mesenteric Artery

Left Colic Appendicular Artery Artery Sigmoid Arteries

Middle Sacral Artery Superior Rectal (Hemorrhoidal) Artery

Inferior Rectal (Hemorrhoidal) Artery

Figure 7 Vascular anatomy.

submucosa and extend to the subserosa of the bowel wall.56 for breast cancer or melanoma, this particular aspect seems As cancer spreads through access to vascular or lymphatic to be refl ected in an unacceptably high false negative rate structures, this is relevant for the management of patients and therefore is one of the key reasons that the methodology with a “cancerous” polyp. The depth of cancer invasion into used for other cancers has not gained any traction for the bowel wall (T stage) is directly associated with the prob- colorectal cancer.58 ability of having nodal disease. A pT1 cancer (which invades the submucosa but not the muscularis propria) carries a 7 to clinical impact: assessment of lymph nodes 10% risk of lymph node metastases. A cancer in a peduncu- An oncologic resection should achieve adequate removal lated polyp that does not reach the basis of the stalk has a of the respective lymph nodes for treatment and for prog- lower risk, whereas a fl at, “cancerous” polyp is immediately nostic aspects. A minimum of 12 lymph nodes should at the level of the lymph vessels and requires appropriate be examined and reported (for each vascular segment) to risk analysis. The paracolic or mesorectal lymph nodes, respectively, are the fi rst level; however, there is no exact determine proper staging of the tumor. With very few demarcation as the lymph node levels seamlessly go over to exceptions (e.g., after radiation), a lesser number of nodes the para-aortic lymph nodes and, in the case of the rectum, may represent either a suboptimal surgery or pathology also to the lateral pelvic sidewall lymph nodes.56 The vis- analysis. Both defi ciencies are problematic as they either ceral network of lymph vessels is not as strictly organized as increase the risk of local recurrence or potentially under- in other anatomic regions and hence is less predictable. In stage the tumor; removal and examination of additional regard to the sentinel lymph node concept, which is relevant lymph nodes may result in stage migration.59–62

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Nervous System is confi rmed by the absence of the rectoanal inhibitory The autonomous enteric nervous system has both sympa- refl ex (RAIR). thetic (inhibitory) and parasympathetic (stimulatory) com- Hirschsprung disease is a disease of childhood or early ponents. The sympathetic nerves originate at levels T6-L3; adulthood, but a few individuals with short segment disease the parasympathetic system has two levels that (a) run in may escape recognition for a long time. Treatment is surgi- the vagal nerve to the small bowel and colon and (b) root in cal and consists of resection of the aganglionic distal 67 S2-S4 for the pelvic structures. In the bowel wall throughout segment, typically with a pull-through reconstruction. the entire gastrointestinal tract [see Figure 8], the Auerbach The dilated proximal colon (which contains normal ganglia) is commonly preserved except if it has functionally ganglionic plexus is located between the longitudinal and decompensated. circular smooth muscle layers and regulates its motility.1 The sympathetic innervation to the rectum is derived The Meissner plexus is located within the inner submucosal from the T6-L3 nerve roots. The superior hypogastric plexus layer of the small and large bowel.1 Its function is more forms behind the IMA and at the sacral promontory branche s multifactorial as it not only regulates bowel motility but is into two bundles. These are known as the hypogastric nerves also associated with intestinal blood fl ow and transport of that run along both sides behind the fascia propria of the ions across the intestinal epithelium.1,63 rectum. The parasympathetic nerves from S2-S4 join at the Hirschsprung disease is the result of a defect in the midlevel pelvis and form a less discriminate autonomic organogenesis when the proximodistal migration of neural nerve plexus that moves from posterior to anterior toward crest cells is not completed.64–66 The congenital lack of the rectum, bladder, prostate, and uterus.14 ganglia (aganglionosis) of the myenteric plexus affects the most distal gastrointestinal tract (rectum, rectosigmoid) and extends proximally to varying degrees.64,67 Deep biopsies are Motility needed to histologically evaluate for the presence or absence of ganglia. It should be noted, however, that even under general characteristics normal circumstances, there is a short segment of 1 to 2 cm Colonic motility is complex and not suffi ciently under- above the dentate line where ganglia may not be detected. stood in detail.68 It depends on an intimate interplay between Functionally in Hirschsprung disease, however, the internal the enteric ganglia and the nonneural interstitial cells of anal sphincter muscle, which represents the continuation Cajal.69 The interstitial cells of Cajal (which, in an oncologic and end of the muscularis propria of the bowel, is always context, are the basis for gastrointestinal stromal tumors affected and lacks the ability to relax appropriately,64 which [GISTs]) are considered pacemaker cells that spontaneously

Sympathetic (Inhibitory) Parasympathetic (Excitatory)

Entero- Mucosa chromaffin Cell

Muscularis Mucosa

Submucosa Submucosal Plexus

Circular Muscle Layer Afferent Neuron Myenteric Nerve Plexus

Interneuron Efferent Logitudinal Muscle Layer Neuron

Serosa

Figure 8 Colonic wall innervation. ACh = acetylcholine; 5-HT = 5-hydroxytryptamine; NE = norepinephrine.

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03/15 gastro anatomy, physiology, and measurement of physiologic function for colorectal surgery — 11 generate electrical slow waves of rhythmic smooth muscle contractions within the colonic wall.70 In addition, they a transmit signals from enteric neurons to smooth muscle cells Anad of the gastrointestinal tract.70 Serotonin and gut hormones Propagation such as cholecystokinin and other enterohumeral peptides (e.g., vasoactive intestinal peptide, neuropeptide Y, peptide YY, and pancreatic polypeptide) are known to have an impact on intestinal and colonic motility in response to meals or distention, but the details remain a focus of investigation.68,71 In contrast to the propulsive small bowel contractions, Orad-Anad Mixing the colonic motility varies more and not only serves at HAPC propulsing the content but also segments and remixes it.68 The activity includes tonic contractions, propagating contractions, and nonpropagating (segmenting) contractions whereby the temporal and spatial sequence is of the utmost importance for the effect. The propulsive contractions consist of low-amplitude propagating contractions (also known as rhythmic phasic contractions) and very forceful high-amplitude propagating contractions (also known as giant migrating propulsions). Low-amplitude propagating contractions are random segmental contractions that are single bursts of motility.72 Giant migrating propulsions start in the ascending colon and serve at moving the stool column toward the rectum,72 whereby descending inhibition allows for relaxation of the receiving segment.68 Colonic motility is stimulated by meals (gastrocolic refl ex) and physical activity but also appears to be subject to a diurnal cycle as the activity decreases during sleep and increases on awakening [see Figure 9].72 The latter seems to be the basis for defecatory urge in the morning.72 b The pharmacologic impacts on colonic motility are numerous, complex, sometimes desired, and frequently unwelcome side effects [see Table 5]. Opioids negatively impact colonic motility and result in constipation or a delayed return of bowel function after abdominal surgery.73 Alvimopan and methylnatrexone are two peripherally acting mu-opioid receptor antagonists73 that do not cross Colonic Activity the blood-brain barrier and hence do not impact the central effects of opioids. However, they do block the impact of Awakening12 pm 12 am Awakening opioids on colonic and small bowel motility.73 Alvimopan and methylnaltrexone have been approved for clinical use Breakfast Lunch Dinner in postsurgical patient care or opioid-induced constipation, Figure 9 (a) The various types of colonic motility: bidirectional respectively,73 even though the practical clinical signifi cance mixing in the proximal colon, unidirectional propagation in the distal beyond statistical signifi cance remains to be tested in view colon, and high-amplitude propagated contractions (HAPCs) over of the additional cost. Neostigmine, a reversible acetylcho- several segments. (b) Colonic activity varies with time of day and is line receptor antagonist, has a parasympathetic effect and most evident on awakening and after meals. can be used to stimulate contractions in Ogilvie syndrome. Thoracic epidural anesthesia with a local anesthetic selec- tively blocks sympathetic nerve roots from T6-L3 and hence shifts the balance toward parasympathetic innervation. The clinical impact: assessment of colonic motility serotonin family appears to increase contractility. Tegaser- od, a partial 5-hydroxytryptamine4 (5-HT4) receptor agonist, Colonic dysmotility can result in constipation, colonic dis- increases the baseline and propulsive contractility of the tention, or diarrhea. In the acute setting (hospital, nursing colon. Prucalopride, a selective, high-affi nity serotonin (5-HT4) home, postsurgical), medications, previous surgeries, inac- receptor agonist with enterokinetic activity, improves tivity, and/or mediastinal or retroperitoneal pathologies colonic motility and stimulates giant migrating propul- are among the frequent triggers of prolonged postoperative sions.74 Linaclotide is a new 14–amino acid peptide agonist ileus (gastric emptying, small bowel) or colonic pseudo- for the guanylyl cyclase C, which is a transmembranous obstruction (Ogilvie syndrome). receptor for heat-stabile enterotoxins on the luminal side In the overwhelming majority of chronic cases, constipa- of intestinal epithelia and triggers secretory diarrhea and tion is either caused by poor dietary habits or the result of increased motility. a morphologic colon obstruction.11,75 Management of such

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Table 5 Mediators and Drugs Affecting Colonic Motility System Agent/Drug Effect Clinical Use Enterohumoral stimulation CCK, neuropeptide Y, peptide Increased postprandial ? YY, pancreatic polypeptide, motility vasoactive intestinal peptide Paraympathicomimetic Neostigmine Increased contraction/ Ogilvie syndrome, ileus (muscarinic receptors) motility Sympathicolytic Thoracic epidural anesthesia Increased motility Postoperative pain management Mu-Opioid antagonist Alvimopan Reduced suppression of Antagonism of postoperative opioid- (peripherally restricted) intestinal activity based pain management Methylnaltrexone Reduced suppression of Chronic opioid-dependent constipation intestinal activity Serotonin Cisapride Increased motility IBS-C

5-HT4 receptor agonists Prucalopride, tegaserod Reduced pain perception Chloride channel–mediated Lubiprostone Secretagogue → accelerated IBS-C, chronic constipation secretagogue colonic transit Guanylate cyclase-C agonist Linaclotide Secretagogue → accelerated IBS-C, chronic constipation colonic transit Glucagon Glucagon, glucagonlike peptide Smooth muscle relaxation Counteract spasticity during colonos- (GLP) copy/anastomosis, pediatric intussusception

Serotonin 5-HT3 antagonist Ramosetron Inhibits motility Withdrawn due to risk of ischemic colitis

CCK = cholecystokinin; 5-HT = 5-hydroxytryptamine; IBS-C = irritable bowel syndrome–constipation. patients requires an age-dependent risk evaluation and Colon Physiology and Metabolism respective assessment of the colon as well as coaching on modifi cations of habits. If those have been checked off general characteristics and the constipation persists, it may be indicated to initiate The colon does not contribute to the absorption of nutri- functional assessments and test the colonic motility and ents. Its two essential functions are to serve as a temporary evacuation11,76: storage area for the body waste and preserve water and 1. Clinical evaluation. A number of instruments have been energy. The colon absorbs water and some electrolytes (in established and validated to defi ne and quantitate the patient’s constipation symptoms to include the Bristol stool scale, the Rome III criteria for irritable bowel syndrome (IBS), or guidelines to defi ne chronic constipation and other functional disorders.77 2. Colonic transit time. Qualitative and (semi)quantitative assessment of the unassisted colonic transit time helps distinguish between normal-transit constipation (IBS-C), slow-transit constipation (colonic inertia), or outlet obstruction (pelvic fl oor dysfunction)76: a. Sitzmark study. Ingestion of radiopaque markers with scheduled x-rays allows for an assessment of the completeness of marker elimination or, in the case of incomplete elimination, distinction of localized versus diffuse distribution patterns [see Figure 10].11 b. Scintigraphy with oral radioisotope markers. This is an alternative (but more infrastructure-dependent) metho d to assess the passage of a radioactive swallow. 3. Morphologic assessment of function. When clinical symptoms (organ prolapse) or a distal distribution pattern in the Sitzmark study suggests an outlet obstruction pattern, morphologic assessment using dynamic pelvic MRI or defecation proctography may be indicated to delineate the nature of the dysfunction and help distinguish single- compartment prolapse (e.g., isolated rectal prolapse), multicompartment pelvic organ prolapse, enterocele, or Figure 10 Assessment of colonic transit by means of a Sitzmark paradoxical puborectalis contraction [see Figure 11].78 study.

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a b

Figure 11 Pelvic organ prolapse on dynamic pelvic magnetic resonance imaging: (a) at rest; (b) on straining.

exchange for others), as well as energy carriers for the colo- follow the electrochemical gradient and diffuse through nocytes.79 The colon, on average, receives 600 to 1,000 mL sodium channels into the cell.80 As sodium diffuses into the (on occasion up to 2 L) of effl uent from the terminal ileum, cell, water follows and is hence absorbed from the feces.79 of which it reabsorbs 60 to 90%, leaving 100 to 300 mL of Two additional mechanisms of sodium uptake are the 80 + + – – – water in the stool. As in the body’s other transmembrane Na /H and Cl /HCO3 exchange and the Cl /butyrate 79 + + – – translocations of molecules, the colonic mechanism also exchange. In animals, a Na /H and Cl /HCO3 exchange relies on a combination of passive or active energy-driven is located on the apical surface of the colonocyte and drives differences in ion concentrations that result in an electro- net sodium absorption. Sodium and chloride are absorbed chemical gradient across the cell membrane.79 On the baso- into the cell by electrolyte-specifi c channels in exchange for – + 80 lateral aspect of the colonocytes (directed to the interstitial excretion of HCO3 and H into the lumen. Whether human space and the blood vessels), a Na+/K+-ATPase pump cell physiology is comparable to the animal models will actively pumps sodium out of the cell with uptake of potas- have to be determined.80 The cystic fi brosis transmembrane sium [see Figure 12].80 As a result, the colonocytes maintain conductance regulator (CFTR) is a protein channel involved a low intracellular sodium concentration such that on the in the physiologic and secretagogue-induced secretion of apical membrane directed to the bowel lumen, sodium ions Cl–. In cystic fi brosis patients, the ability to secrete chloride

Cl Na Cl Na Cl AE1 NHE3 DRA ENaC CFTR K HCO3 HOHNa Cl Paracellular Paracellular Cl 3Na K Cl NKA

AE1/2 ATP NKCC1 Na Na 2Cl K HCO3 2K

Figure 12 Electrolyte transport mechanisms within the colonocyte. AE = anion exchanger; ATP = adenosine triphosphate; CFTR = cystic ﬁ bro- + sis transmembrane conductance regulator; DRA = “downregulated in adenoma”exchanger; EnaC = epithelial Na channel; HCO3 = bicarbonate; NHE3 = Na+/H+ exchanger; NKA = Na+/K+ ATPase; NKCC1 = Na+-2Cl–K+ cotransporter.

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03/15 gastro anatomy, physiology, and measurement of physiologic function for colorectal surgery — 14 is reduced or absent and affects several organ systems. In gender variation).14 The anatomic and histologic anal canal the gastrointestinal tract, it results in meconium-ileus in 10% entails the distance from the anal verge to the anal transi- of newborns and meconium-equivalent at a later age.81 tional zone 6 to 12 mm above the dentate line.14 The micro- The Cl–/butyrate exchange is based on short-chain fatty scopic anatomy of the anal canal is defi ned in relation to acids (SCFAs) that are believed to stimulate sodium absorp- the dentate line, which marks the embryologic fusion zone tion.80,82,83 Butyrate and chloride are absorbed across the between endo- and ectoderm. The anal transitional zone membrane, whereas bicarbonate is released.80 (also known as the cloacogenic zone) refl ects the change The absorption of luminal effl uent can be increased up to from single-layer columnar colonic mucosa to a multilayer 5 to 6 L per day, primarily when aldosterone is present.79 cuboidal, transitional, and squamocolumnar pattern.88 Aldosterone stimulates the upregulation of sodium channels The transition zone coincides with a bluish color due to the on the colonocyte membrane, which allows for increased underlying hemorrhoidal plexus.89 Just below the dentate sodium/water absorption.80,84 line, the so-called anoderm has squamous epithelium but The colonocyte obtains 60% of its energy from the luminal lacks skin appendages (hair follicles, apocrine glands) in the content in a symbiotic relationship with intraluminal bacte- fi rst segment.88 Outside the anal verge, skin appendages ria. The colon is colonized with over 400 species of bacteria are present, the epithelium becomes thicker and more that serve an essential function in colonic metabolism pigmented, and the skin creates a radial pattern.89 The term (microbiome).85,86 There are 1012 bacteria per gram of wet anal margin is frequently used but poorly defi ned and much feces.84 Most of the bacteria are anaerobes, but there are less needed: it refers to the skin outside the anal verge up to also aerobes and gram-positive and gram-negative bacteria. a virtual perimeter border of approximately 5 cm.11,14 Bacteroides is the most common anaerobe bacterium and Under normal circumstances, the dentate line is located Escherichia coli the most common aerobe bacterium in approximately 1 to 2 cm above the anal verge. Correlating the colon. with the wide rectal reservoir narrowing to the anal canal, These bacteria ferment insoluble carbohydrates, creating the last segment is characterized by a circumferential 79,82 SCFAs, the primary energy source for the colonocyte. arrangement of axial mucosal folds, the columns of 79 Acetate, propionate, and butyrate are the primary SCFAs. Morgagni.14 The anal crypts are located at the base between Butyrate is the major energy source for the colonocyte, two adjacent columns (i.e., at the dentate line) and refl ect the although it accounts for only 20% of all the SCFAs in the entry point of the anal glands. These glands, whose function 80 colon. Furthermore, butyrate is thought to inhibit colonic is unknown in humans, are variable in number (four to infl ammation and carcinogenesis, decrease oxidative dam- eight) and traverse the internal anal sphincter to the inter- age to the colonic mucosa, and aid in colonocyte growth sphincteric space.14 These cryptoglandular complexes in the 79,80 and differentiation. Absence of SCFAs as a result of fecal overwhelming majority of cases appear to be the origin of diversion results in a loss of mucosal integrity (diversion perirectal abscess and fi stula formation. colitis/proctitis). As previously mentioned, the dentate line refl ects not clinical impact: diarrhea only a histologic transition zone but also the border between predominantly visceral and strictly somatic blood supply, Diarrhea, defi ned as too loose or too frequent stools, can lymph drainage, and innervation.11,14 Proximal to the dentate be triggered by numerous causes (e.g., infectious, dietary, line, the arterial blood supply derives from the superior toxic, pharmacologic, intrinsic/enterohumeral, hypermotil- hemorrhoidal/rectal artery (the terminal branch of the IMA), ity). They result in a number of isolated imbalances or, in conjunction with the much smaller middle hemorrhoidal more frequently, combinations thereof, such as increased artery that branches off the internal iliac artery. Submucosal motility, exhausted absorptive capacity of the colon (due to hemorrhoidal plexus forms the hemorrhoidal cushions excessive volume of small bowel effl uent), increased colonic (internal hemorrhoids) above the dentate line; when not secretion versus insuffi cient absorption, or physical mucosal enlarged, these cushions are an important component of the damage.79 Heat-stabile enterotoxins are able to stimulate continence mechanism as they add to the fi ne-tuning of the the transmembranous receptor guanylyl cyclase C and anal canal seal. Sensory nerve fi bers run within the auto- trigger secretory diarrhea. Non–toxin-producing strands nomic nerve plexus and transmit signals on bowel disten- of Clostridium diffi cile are commensal colonic bacteria. tion but to a much lesser degree on pain. For that reason, However, acquisition of virulent strands producing toxins management of internal hemorrhoids above the dentate line A (enterotoxic) and/or B (cytotoxic) can result in a broad (e.g., banding, stapled hemorrhoidectomy) is associated spectrum of clinical presentations, from asymptomatic car- with comparably less pain.90,91 rier, to chronic diarrhea without morphologic abnormality, In contrast, the anal canal distal to the dentate line is to pseudomembranous colitis or deadly fulminant colitis.87 supplied by branches of the internal iliac artery only, that is, the middle and inferior hemorrhoidal artery, the latter Anal Canal Anatomy of which branches off from the internal pudendal artery. The venous drainage follows the arterial supply but has general characteristics extensive collaterals. The external hemorrhoidal plexus have Defi nitions of the anal canal vary considerably between variable junctions to the internal hemorrhoidal plexus. This anatomists and surgeons.14 The surgical anal canal refl ects area of the anal canal (particularly the skin) is richly inner- the digital rectal examination and extends from the anal vated by pain fi bers, which explains that external patholo- verge to the upper level of the puborectalis sling; it mea- gies (thrombosed external hemorrhoids, abscess, fi ssure, sures, on average, 2 to 4 cm (with substantial individual and surgical wound) are associated with substantial pain.

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Lymphatic drainage is also divided at the dentate line: (1) to and form the funnel-shaped musculotendinous termination the mesorectal and pelvic lymph nodes (above the dentate of the pelvic outlet.14 It supports the abdominal and pelvic line) and (2) to the inguinal and/or internal iliac lymph organs but allows passage of the anorectal and urogenital nodes (below the dentate line). viscera through two separate hiatal openings14,93; furthermore, the pelvic fl oor is an important component for clinical impact: distinction between different both control and evacuation processes. Separate units of the anorectal cancers levator ani complex are identifi ed from lateral to medial Cancer staging and treatment vary considerably between as the ischiococcygeus, iliococcygeus, pubococcygeus, and rectal cancer, anal cancer, or “anal margin” cancers: puborectalis muscles. The anococcygeal raphe, a fi brous condensation, serves as muscle insertion in the posterior 1. Perianal cancers can be seen in their entirety without midline. The puborectalis muscle has an anterior insertion instrument help and are assessed and treated as skin and forms a U-shaped sling around the upper anal canal cancers. (anorectal angle); it is cephalad to and transitions into the 2. Anal canal cancer (“anal cancer”) refers to tumors of deep component of the external anal sphincter muscle; both mostly squamous cells but occasionally adenocarcinoma muscles are innervated by the inferior rectal nerve, a branch (arising from the anal or skin glands, occasionally from of the pudendal nerve.14 fi stulous tracts) whose center and origin appear to be The gastrointestinal tube merges into the lowest point of distal to the dentate line and/or that cannot be visualized the pelvic fl oor and forms the cylindrical anal canal with in their entirety without instrumentation because they are muscle components of the striated skeletal pelvic fl oor located and at least in part hidden within the anal canal (puborectalis and external sphincter muscles) as well as the (proximal to the anal verge). The staging follows the TNM smooth muscle visceral muscularis propria; as that layer guidelines and is based on tumor size (T), lymph node continues, it condenses to form the internal anal sphincter, involvement (N), and distant metastases (M) whereby the which is innervated by autonomic sympathetic (L5) and inguinal lymph nodes are relevant sites of progressive parasympathetic (S2-S4) nerves. The external anal sphincter disease. is innervated by the inferior pudendal nerve, a branch of 3. Rectal cancers are mostly adenocarcinoma (rarely adeno- S2-S4. The internal anal sphincter ends below the dentate squamous or even squamous cell carcinoma) that origi- line but before the external sphincter, which results in a nate above the dentate line but with increasing size may palpable intersphincteric groove.11,88 expand to and through the anal canal. The staging according to the TNM system is based on depth of invasion (T), perirectal/pelvic lymph node involvement (N), Anorectal Physiology: Continence and Defecation and distant metastases (M). 4. Nonepithelial tumors (melanoma, carcinoid, lymphoma) general characteristics are assessed and treated according to specifi c guidelines. Both continence and defecation seem to be simple events but in reality rely on a subtle interplay of structural and functional components.11,14 The peristaltic wave propulses Musculature of the Pelvis the stool toward the rectum, where it is stored until a defeca- An arrangement of several muscles provides structural tion is desired and initiated.94 Control relies on a functional support and functional closure of the pelvis and gastrointes- and modifi able outlet resistance, which is generated by the tinal tract [see Table 6]. They can be divided into (1) muscles previously mentioned muscular structures; in addition, the that line the sidewalls of the osseous pelvis, (2) muscles capacity and compliance of the rectal reservoir (storage area) of the pelvic fl oor, and (3) muscles of the anal sphincter and the stool consistency are relevant elements. The internal complex.14,92 anal sphincter and the combination of external anal sphinc- The pelvic fl oor (pelvic diaphragm) is a composite muscle ter and puborectalis muscle contribute to the generation of consisting of several subunits that are innervated by branche s the resting pressure at 50 to 80% and 20 to 30%, respectively. of the primary ventral branches of the spinal nerves S3-S4 On demand, the external anal sphincter and the puborectalis

Table 6 Pelvic Floor Muscles Muscle Type and Innervation Function Contribution ERUS Appearance Levator ani: ischiococcy- Skeletal/striated Support of abdominal Anorectal White (hyperechogenic), parabolic shape geus, iliococcygeus, and pelvic organs, angulation pubococcygeus, anorectal angle puborectalis External anal sphincter Skeletal/striated Involuntary and Resting tone White (hyperechogenic), outer ring, muscle voluntary extends from lower end of puborectalis Slow twitch — Squeeze tone muscle to distal anal canal Internal anal sphincter Smooth muscle Involuntary Resting tone Black (hypoechogenic) inner ring; extends muscle from lower end of puborectalis muscle to midanal canal

ERUS = endorectal ultrasound.

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03/15 gastro anatomy, physiology, and measurement of physiologic function for colorectal surgery — 16 muscle can substantially increase the pressure but typically numerous mechanisms (e.g., injury, surgery, nerve damage, cannot maintain the incremental squeeze level for more than degeneration).96 Loss of rectal sensation may represent 1 minute. a localized phenomenon or be part of systemic or regional Distention in the rectum triggers the involuntary smooth neuropathy; as a result, the urge to defecate may be muscles of the internal anal sphincter to relax, while, in diminished. response, the external sphincter contracts.94,95 This RAIR is Pelvic organ malposition and discoordination of the pel- considered a sampling refl ex to allow for discrimination vic fl oor muscles are common pathophysiologic mechanisms between gas, liquid, or solid stool.94 If a defecation is permit- to negatively interfere with the normal fl ow of defecation. ted, the puborectalis muscle sling relaxes, hence straighten- Pelvic organ prolapse may cause physical obstructions ing the anorectal angle; at the same time, Valsalva maneuvers (intussusception) or result in kinks that are aggravated increase the abdominal pressure to support the increased by positional gravity or Valsalva maneuvers. Functional rectal contractility and propulsion. The pelvic fl oor descends, problems include contraction rather than relaxation of the and both the internal and external anal sphincter muscles puborectalis muscle during attempted evacuation, which relax such that the stool can be evacuated.94 If defecation decreases the anorectal angle and increases the outlet is to be deferred, the external sphincter and puborectalis obstruction (obstructed defecation). In the longer run, the muscles contract, hence dramatically increasing the outlet chronic spasticity may be associated with chronic pelvic resistance, while the rectum relaxes to accommodate more pain (levator ani spasm), which can be replicated by lateral stool in the rectal vault.94,95 tenderness to palpation on the levator muscles on digital rectal examination. clinical impact: incontinence and obstructed defecation Anophysiology Testing Disturbances or imbalances of the three core components of fecal control (stool consistency, rectal reservoir capacity general characteristics and compliance, functional sphincter complex) may contrib- A good history and a physical anorectal examination can ute to the development of incontinence.11,94 Alteration of the often defi ne the nature of a functional problem quite well. stool consistency (diarrhea) and volume may overcome the Nonetheless, for medical and potentially legal reasons, it rectal capacity and exhaust the sphincter resistance, leading might be desirable to obtain objective parameters to support to fecal incontinence.96 The rectal capacity and compliance the clinical impression. Anophysiology testing, which con- may be impaired by proctitis or fi brosis (e.g., infl ammatory sists of a number of modules [see Table 7], aims at analyzing bowel disease, radiation exposure, surgery).96 Furthermore, the anorectal function and morphology and defi ning factors the sphincter function can suffer a negative impact through contributing to incontinence and/or constipation11:

Table 7 Anophysiology Testing Test Purpose Normal Values Interpretation Indication Pudendal nerve mo- Nerve conductiv- < 2.5 ms Pudendal neuropathy? Potential prognostic parameter tor terminal ity for sphincteroplasty latency (PNMTL) Manometry Absolute values, pressure Objective data prior to treatment Resting Resting tone 50–100 mm Hg profile, length, Squeeze Squeeze tone 100–350 mm Hg asymmetry RAIR Reflex circle Present Present = normal; absent Presence → HD and Chagas = different reasons disease ruled out Anorectal volume Sensory function FS 10–50 mL Abnormal/normal Megarectum/rectocele, sensation Rectal capacity FU 50–150 mL volume? strictured/scarred rectum, IBS MTV 140–440 mL Rectal compliance Reservoir function 2–6 mL/mm Hg Abnormal/normal Megarectum/rectocele, compliance? strictured/scarred rectum, IBS EMG Neuromotor unit Baseline Normal sequence, Constipation workup, Increase with squeeze/cough paradoxical contraction occasional assessment of Decrease with strain sphincter contractility Balloon expulsion Neuromuscular Success Success vs. failure May suggest need for defecogra- and content phy or MRI coordination ERUS Normal vs. Puborectalis sling Intact, normal thickness, Segmental defect? Fragmenta- pathological EAS circumferential normal echogenicity tion? Scarring? anatomy IAS circumferential

EAS = external anal sphincter; EMG = electromyography; ERUS = endorectal ultrasonography; FS = fi rst sensation; FU = fi rst urge; HD = Hirschsprung disease; IAS = internal anal sphincter; MRI = magnetic resonance imaging; MTV = maximal tolerable volume; RAIR = rectoanal inhibitory refl ex.

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1. Muscle strength. Anorectal manometry evaluates the tone 5. Morphology. Anorectal ultrasonography (and less com- of the sphincter muscle at rest and during squeezing at monly MRI) is performed to assess the integrity of the multiple levels throughout the anal canal, defi nes the components of the puborectalis and internal and external length and profi le of the high-pressure zone, and, on sphincters and weaknesses or defects. occasion, may provide information about asymmetries as clues for underlying defects. clinical impact: sacral nerve stimulation 2. Neuromuscular function. Several components can be Treatment options for fecal incontinence, include, among assessed according to the specifi c needs and may provide others, sacral nerve stimulation, which entails a two-stage different aspects of information. procedure to continuously stimulate the S3 nerve root. a. Perianal sensation and anal wink are both part of the The fi rst stage is primarily for diagnostic and prognostic clinical examination and can be assessed by means of purposes but already places a lead with four stimulatory a cotton swab. They provide basic information about subunits into the S3 foramen. Correct placement allows the intactness and symmetry of the innervation. for obtaining a visible motor response on the pelvic fl oor b. Pudendal nerve terminal motor latency (PNTML) mea- (bellow sign) and the toes. If this temporary electrode, which sures the conductivity of the pudendal nerve between is connected to an external stimulator, results in at least 50% a stimulus site and the reading site on the sphincter improvement in the incontinence symptoms, the second 94 complex ; prolonged PNTML is interpreted as a sign procedure 2 weeks later implants a defi nitive stimulator. of pudendal neuropathy. The treatment has been remarkably successful even though c. Anorectal volume sensation is assessed by incremental the exact mechanism of action remains unclear. It has been injection of fl uid into a rectal balloon to determine the speculated that the stimulation modulates the rectal sensa- respective volumes for (a) fi rst sensation, (b) fi rst urge tion, stimulates and modulates via the afferent pathways the 96 to defecate, and (c) the maximal tolerable volume. associated brain activity, or potentially initiates a retrograde The volume is typically correlated to the pressure peristaltic wave.97 and allows for calculation of the rectal compliance. Excessive volume tolerance may provide a clue to underlying sensory neuropathy; reduced volume tol- Summary erance suggests either a diminished or rigid reservoir A thorough understanding of the colorectal and anorectal function (low compliance) or irritable bowel syndrome anatomy and physiology represents the basis for the clini- (low-volume tolerance with normal rectal compliance). cian to develop a meaningful differential diagnosis, defi ne d. During RAIR, the rectal balloon is rapidly fi lled with and initiate appropriate tests, and carry out successful surgi- air to trigger the refl exive relaxation of the internal cal interventions. It should be cautioned, however, that the sphincter. The presence of this refl ex rules out individual settings may vary considerably and that more Hirschprung or Chagas disease, whereas its absence detailed information may need to be gathered. is necessary but not suffi cient to confi rm either diagnosis. Financial Disclosures: Nicole Lamb, MD, and Andreas M. Kaiser, MD, FACS, e. Anorectal electromyography (EMG) is occasionally FASCRS, have no relevant fi nancial relationships to disclose. used to evaluate neuromuscular motor units of the sphincter complex.96 It can be carried out either as more precise but also more uncomfortable needle EMG References or more commonly as surface EMG that only records 1. Butler Tjaden NE, Trainor PA. The developmental etiology the summary effect of activity. Under normal circum- and pathogenesis of Hirschsprung disease. Transl Res 2013; stances, the baseline activity should change to an 162:1–15. increase during squeezing or coughing, whereas it 2. Park Y-K, Franklin JL, Settle SH, et al. Gene expression should decrease on straining.96 The test has little profi le analysis of mouse colon embryonic development. impact for evaluation of fecal incontinence but may Genesis 2005;41:1–12. be helpful in patients complaining of constipation. 3. Sakorafas GH, Zouros E, Peros G. Applied vascular Nonrelaxing puborectalis muscles are demonstrated anatomy of the colon and rectum: clinical implications for by a paradoxical increase in activity during straining.11 the surgical oncologist. Surg Oncol 2006;15:243–55. 3. Reservoir function. The storage function of the rectum is 4. Herman RS, Teitelbaum DH. Anorectal malformations. Clin assessed by means of the rectal capacity and compliance Perinatol 2012;39:403–22. (see above). Both parameters may have decreased as a 5. Alamo L, Meyrat BJ, Meuwly JY, et al. Anorectal malforma- result of various disease processes or treatments (surgery, tions: fi nding the pathway out of the labyrinth. Radiograph- radiation) or increased (e.g., in the presence of a large ics 2013;33:491–512. rectocele or a megarectum). 6. Irving MH, Catchpole B. ABC of colorectal diseases. 4. Evacuatory function. Balloon expulsion is a very simple Anatomy and physiology of the colon, rectum, and anus. and cheap tool to assess the patient’s ability to coordinate BMJ 1992;304:1106–8. the complexity of different defecatory components and 7. Schumpelick V, Dreuw B, Ophoff K, et al. Appendix and eliminate the balloon. In cooperative patients, it helps cecum. Embryology, anatomy, and surgical applications. rule out relevant pelvic fl oor dyssynergia (i.e., the disco- Surg Clin North Am 2000;80:295–318. ordination of rectum, abdominal, and pelvic fl oor muscles 8. Corman ML. Corman’s colon and rectal surgery. 6th ed. during defecation). Philadelphia: Lippincott Williams and Wilkins; 2013.

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9. Juul T, Ahlberg M, Biondo S, et al. International validation 27. Beaugerie L, Sokol H. Appendicitis, not appendectomy, is of the low anterior resection syndrome score. Ann Surg protective against ulcerative colitis, both in the general 2014;259:728–34. population and fi rst-degree relatives of patients with IBD. 10. Fazio VW, Zutshi M, Remzi FH, et al. A randomized Infl amm Bowel Dis 2010;16:356–7. multicenter trial to compare long-term functional outcome, 28. Frisch M, Rostgaard C. Appendectomy and ulcerative quality of life, and complications of surgical procedures colitis. Epidemiology 2005;16:131–2. for low rectal cancers. Ann Surg 2007;246:481–8; discussion 29. Andersson RE, Olaison G, Tysk C, et al. Appendectomy and 488–90. protection against ulcerative colitis. N Engl J Med 2001; 11. Kaiser AM. McGraw-Hill manual colorectal surgery. 1st ed. 344:808–14. New York: McGraw-Hill; 2009. 30. Slam KD, Calkins S, Cason FD. LaPlace’s law revisited: 12. Egorov VI, Schastlivtsev IV, Prut EV, et al. Mechanical cecal perforation as an unusual presentation of pancreatic properties of the human gastrointestinal tract. J Biomech carcinoma. World J Surg Oncol 2007;5:14. 2002;35:1417–25. 31. Saunders BP, Phillips RK, Williams CB. Intraoperative 13. Edge SB, Byrd DR, Compton CC, et al. AJCC cancer staging measurement of colonic anatomy and attachments with manual. New York: Springer; 2010. relevance to colonoscopy. Br J Surg 1995;82:1491–3. 14. Kaiser AM, Ortega AE. Anorectal anatomy. Surg Clin North 32. West NP, Hohenberger W, Weber K, et al. Complete meso- Am 2002;82:1125–38. colic excision with central vascular ligation produces an 15. Kaiser AM, Beart RW. Images in clinical medicine. Chronic oncologically superior specimen compared with standard ulcerative colitis with megacolon. N Engl J Med 2003;349: surgery for carcinoma of the colon. J Clin Oncol 2010;28: 358. 272–8. 16. Rashid A, Nazir S, Hakim SY, et al. Epiploic appendagitis 33. Hemming J, Floch M. Features and management of colonic of caecum: a diagnostic dilemma. Ger Med Sci 2012;10: diverticular disease. Curr Gastroenterol Rep 2010;12: Doc14. DOI: 10.3205/000165. [Epub 2012 Oct 30] 399–407. 17. Levin B, Lieberman DA, McFarland B, et al. Screening and 34. Kaiser AM, Jiang JK, Lake JP, et al. The management surveillance for the early detection of colorectal cancer and of complicated diverticulitis and the role of computed tomography. Am J Gastroenterol 2005;100:910–7. adenomatous polyps, 2008: a joint guideline from the 35. Nelson H, Petrelli N, Carlin A, et al. Guidelines 2000 for American Cancer Society, the US Multi-Society Task colon and rectal cancer surgery. J Natl Cancer Inst 2001; Force on Colorectal Cancer, and the American College of 93:583–96. Radiology. CA Cancer J Clin 2008;58:130–60. 36. Bennett AE. Correlative anatomy of the anus and rectum. 18. Friedman A, Lance P. AGA position statement of computed Semin Ultrasound CT MR 2008;29:400–8. tomographic colonography. Gastroenterology 2007;132: 37. Lake JP, Essani R, Petrone P, et al. Management of retained 1632–3. colorectal foreign bodies: predictors of operative interven- 19. Randal Bollinger R, Barbas AS, Bush EL, et al. Biofi lms in tion. Dis Colon Rectum 2004;47:1694–8. the large bowel suggest an apparent function of the human 38. Church JM, Raudkivi PJ, Hill GL. The surgical anatomy vermiform appendix. J Theor Biol 2007;249:826–31. of the rectum—a review with particular relevance to the 20. Deshmukh S, Verde F, Johnson PT, et al. Anatomical vari- hazards of rectal mobilisation. Int J Colorectal Dis 1987;2: ants and pathologies of the vermix. Emerg Radiol 2014; 158–66. 21:543–52. DOI: 10.1007/s10140-014-1206-4. [Epub 2014 39. Heald RJ. The ‘Holy Plane’ of rectal surgery. J R Soc Med Feb 26] 1988;81:503–8. 21. Wakeley CP. The position of the vermiform appendix as 40. Beart RW Jr. Mesorectal excision for rectal carcinoma: the ascertained by an analysis of 10,000 cases. J Anat 1933;67: new standard? Adv Surg 1999;32:193–203. 277–83. 41. Jass JR, O’Brien J, Riddell RH, et al. Recommendations for 22. Mariadason JG, Wang WN, Wallack MK, et al. Negative the reporting of surgically resected specimens of colorectal appendicectomy rate as a quality metric in the management carcinoma: Association of Directors of Anatomic and of appendicitis: impact of computed tomography, Alvarado Surgical Pathology. Am J Clin Pathol 2008;129:13–23. score and the defi nition of negative appendicectomy. Ann 42. Enker WE, Kafka NJ, Martz J. Planes of sharp pelvic dissec- R Coll Surg Engl 2012;94:395–401. tion for primary, locally advanced, or recurrent rectal 23. Spanos CP, Asteriou S, Baddour A, et al. Infarction of the cancer. Semin Surg Oncol 2000;18:199–206. ileocecal fold of Treves: a case of right lower quadrant pain. 43. Quirke P, Steele R, Monson J, et al. Effect of the plane Surg Laparosc Endosc Percutan Tech 2008;18:98–101. of surgery achieved on local recurrence in patients with 24. Im GY, Modayil RJ, Lin CT, et al. The appendix may protect operable rectal cancer: a prospective study using data from against Clostridium diffi cile recurrence. Clin Gastroenterol the MRC CR07 and NCIC-CTG CO16 randomised clinical Hepatol 2011;9:1072–7. trial. Lancet 2009;373:821–8. 25. Laurin M, Everett ML, Parker W. The cecal appendix: one 44. Crapp AR, Cuthbertson AM. William Waldeyer and the more immune component with a function disturbed by rectosacral fascia. Surg Gynecol Obstet 1974;138:252–6. post-industrial culture. Anat Rec (Hoboken) 2011;294: 45. Yeung JM, Ferris NJ, Lynch AC, et al. Preoperative staging 567–79. of rectal cancer. Future Oncol 2009;5:1295–306. 26. Gardenbroek TJ, Eshuis EJ, Ponsioen CI, et al. The effect 46. Havenga K, Grossmann I, DeRuiter M, et al. Defi nition of of appendectomy on the course of ulcerative colitis: a total mesorectal excision, including the perineal phase: systematic review. Colorectal Dis 2012;14:545–53. technical considerations. Dig Dis 2007;25:44–50.

Scientiﬁ c American Surgery

03/15 gastro anatomy, physiology, and measurement of physiologic function for colorectal surgery — 19

47. Heald RJ, Moran BJ, Ryall RD, et al. Rectal cancer: the 66. Langer JC. Hirschsprung disease. Curr Opin Pediatr 2013; Basingstoke experience of total mesorectal excision, 1978– 25:368–74. 1997. Arch Surg 1998;133:894–9. 67. Chen Y, Nah SA, Laksmi NK, et al. Transanal endorectal 48. Kapiteijn E, Marijnen CA, Nagtegaal ID, et al. Preoperative pull-through versus transabdominal approach for radiotherapy combined with total mesorectal excision for Hirschsprung’s disease: a systematic review and meta- resectable rectal cancer. N Engl J Med 2001;345:638–46. analysis. J Pediatr Surg 2013;48:642–51. 49. Swedish Rectal Cancer Trial. Improved survival with 68. Sarna SK. Colonic motility: from bench side to bedside. San preoperative radiotherapy in resectable rectal cancer. Rafael (CA): Morgan & Claypool Life Sciences; 2010. Swedish Rectal Cancer Trial. N Engl J Med 1997;336:980–7. 69. Zhang RX, Wang XY, Chen D, et al. Role of interstitial cells 50. Kaiser AM, Klaristenfeld D, Beart RW. Preoperative versus of Cajal in the generation and modulation of motor activity postoperative radiotherapy for rectal cancer in a decision induced by cholinergic neurotransmission in the stomach. analysis and outcome prediction model. Ann Surg Oncol Neurogastroenterol Motil 2011;23:e356–71. 2012;19:4150–60. 70. Klein S, Seidler B, Kettenberger A, et al. Interstitial cells of 51. Kim NK. Anatomic basis of sharp pelvic dissection for cura- Cajal integrate excitatory and inhibitory neurotransmission tive resection of rectal cancer. Yonsei Med J 2005;46:737–49. with intestinal slow-wave activity. Nat Commun 2013;4: 52. Patel UB, Taylor F, Blomqvist L, et al. Magnetic resonance 1630. imaging-detected tumor response for locally advanced 71. Tack J, Vanden Berghe P. Neuropeptides and colonic rectal cancer predicts survival outcomes: MERCURY motility: it’s all in the little brain. Gastroenterology 2000; experience. J Clin Oncol 2011;29:3753–60. 119:257–60. 53. Nagtegaal ID, Quirke P. What is the role for the circumfer- 72. Bassotti G, Crowell MD, Whitehead WE. Contractile ential margin in the modern treatment of rectal cancer? activity of the human colon: lessons from 24 hour studies. J Clin Oncol 2008;26:303–12. Gut 1993;34:129–33. 54. Brown G. Thin section MRI in multidisciplinary pre- 73. Gras B, Magge S, Bloom A, et al. Motility disorders of the operative decision making for patients with rectal cancer. colon and rectum. Curr Opin Gastroenterol 2013;29:66–71. Br J Radiol 2005;78 Spec No 2:S117–27. 74. Hoffman JM, Tyler K, MacEachern SJ, et al. Activation of 55. Munoz E, Granero-Castro P, Frasson M, et al. Modifi ed colonic mucosal 5-HT(4) receptors accelerates propulsive Wong’s classifi cation improves the accuracy of rectal cancer motility and inhibits visceral hypersensitivity. Gastroenter- staging by endorectal ultrasound and MRI. Dis Colon ology 2012;142:844–54 e844. Rectum 2013;56:1332–8. 75. Bharucha AE, Dorn SD, Lembo A, et al. American Gastro- 56. Hollinshead WH. Embryology and surgical anatomy of the enterological Association medical position statement on colon. Dis Colon Rectum 1962;5:23–7. constipation. Gastroenterology 2013;144:211–7. 57. Griffi ths JD. Surgical anatomy of the blood supply of the 76. Locke GR 3rd, Pemberton JH, Phillips SF. American Gastro- distal colon. Ann R Coll Surg Engl 1956;19:241–56. enterological Association medical position statement: 58. Bertagnolli M, Miedema B, Redston M, et al. Sentinel node guidelines on constipation. Gastroenterology 2000;119: staging of resectable colon cancer: results of a multicenter 1761–6. study. Ann Surg 2004;240:624–8; discussion 628–30. 77. Shekhar C, Monaghan PJ, Morris J, et al. Rome III functional 59. Willaert W, Mareel M, Van De Putte D, et al. Lymphatic constipation and irritable bowel syndrome with constipa- spread, nodal count and the extent of lymphadenectomy in tion are similar disorders within a spectrum of sensitiza- cancer of the colon. Cancer Treat Rev 2014;40:405–13. tion, regulated by serotonin. Gastroenterology 2013;145: 60. Shi Q, Andre T, Grothey A, et al. Comparison of outcomes 749–57; quiz e713–44. after fl uorouracil-based adjuvant therapy for stages II 78. Maccioni F. Functional disorders of the ano-rectal compart- and III colon cancer between 1978 to 1995 and 1996 to 2007: ment of the pelvic fl oor: clinical and diagnostic value of evidence of stage migration from the ACCENT database. dynamic MRI. Abdom Imaging 2013;38:930–51. J Clin Oncol 2013;31:3656–63. 79. Milla PJ. Advances in understanding colonic function. 61. Lykke J, Roikjaer O, Jess P, et al. The relation between J Pediatr Gastroenterol Nutr 2009;48 Suppl 2:S43–5. lymph node status and survival in stage I-III colon cancer: 80. Sandle GI. Salt and water absorption in the human colon: a results from a prospective nationwide cohort study. modern appraisal. Gut 1998;43:294–9. Colorectal Dis 2013;15:559–65. 81. Greger R. Role of CFTR in the colon. Annu Rev Physiol 62. Nissan A, Protic M, Bilchik AJ, et al. United States Military 2000;62:467–91. Cancer Institute Clinical Trials Group (USMCI GI-01) 82. Donohoe DR, Garge N, Zhang X, et al. The microbiome and randomized controlled trial comparing targeted nodal butyrate regulate energy metabolism and autophagy in the assessment and ultrastaging with standard pathological mammalian colon. Cell Metab 2011;13:517–26. evaluation for colon cancer. Ann Surg 2012;256:412–27. 83. Musch MW, Bookstein C, Xie Y, et al. SCFA increase intes- 63. Hayashi H, Suzuki T, Yamamoto T, et al. Cholinergic tinal Na absorption by induction of NHE3 in rat colon and inhibition of electrogenic sodium absorption in the guinea human intestinal C2/bbe cells. Am J Physiol Gastrointest pig distal colon. Am J Physiol Gastrointest Liver Physiol Liver Physiol 2001;280:G687–93. 2003;284:G617–28. 84. Beck DE, Roberts PL, Saclarides TJ, et al. The ASCRS 64. Gourlay DM. Colorectal considerations in pediatric patients. textbook of colon and rectal surgery. 2nd ed. New York: Surg Clin North Am 2013;93:251–72. Springer Science+Business Media LLC; 2011. 65. Butler Tjaden NE, Trainor PA. The developmental etiology 85. Mayer EA, Savidge T, Shulman RJ. Brain-gut microbiome and pathogenesis of Hirschsprung disease. Transl Res 2013; interactions and functional bowel disorders. Gastroenterol- 162:1–15. ogy 2014;146:1500–12.

Scientiﬁ c American Surgery

03/15 gastro anatomy, physiology, and measurement of physiologic function for colorectal surgery — 20

86. Zackular JP, Baxter NT, Iverson KD, et al. The gut microbi- 93. Strohbehn K. Normal pelvic ﬂ oor anatomy. Obstet Gynecol ome modulates colon tumorigenesis. mBio 2013;4:e00692–13. Clin North Am 1998;25:683–705. 87. Dudukgian H, Sie E, Gonzalez-Ruiz C, et al. C. difﬁ cile 94. Thorson AG. Anorectal physiology. Surg Clin North Am colitis—predictors of fatal outcome. J Gastrointest Surg 2002;82:1115–23. 2010;14:315–22. 95. Bharucha AE. Update of tests of colon and rectal structure 88. Dujovny N, Quiros RM, Saclarides TJ. Anorectal anatomy and function. J Clin Gastroenterol 2006;40:96–103. and embryology. Surg Oncol Clin N Am 2004;13:277–93. 89. Godlewski G, Prudhomme M. Embryology and anatomy 96. Rasmussen OO. Anorectal function. Dis Colon Rectum of the anorectum. Basis of surgery. Surg Clin North Am 1994;37:386–403. 2000;80:319–43. 97. Kaiser AM, Orangio GR, Zutshi M, et al. Current status: 90. Nunoo-Mensah JW, Kaiser AM. Stapled hemorrhoidec- new technologies for the treatment of patients with fecal tomy. Am J Surg 2005;190:127–30. incontinence. Surg Endosc 2014;28:2277–301. 91. Balasubramaniam S, Kaiser AM. Management options for symptomatic hemorrhoids. Curr Gastroenterol Rep 2003;5: 431–7. Acknowledgment 92. Ger R. Surgical anatomy of the pelvis. Surg Clin North Am 1988;68:1201–16. Figures 4, 5, 7, 8, 9, and 12 Karen Williams

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