DEVELOPMENT OF THE GASTROINTESTINAL SYSTEM:  HINDGUT

By Bruce I. Bogart, Ph.D.

I. Introduction
II. Anatomical Considerations
III. CONGENITAL ABNORMALITIES OF THE HINDGUT
  A. Urorectal Septal Defects
  B. Low Anorectal Defects
  C. High Anorectal Defects
  D. Congenital Aganglionic Megacolon (Hirschsprung's Disease)
STUDY QUESTIONS

I.  Introduction

The hindgut extends from the midgut (middle of transverse colon) to the body wall and is supplied by the inferior mesenteric artery (S-Fig. 13.4/14.4, 13.5/14/5).  The hindgut consists of the developing distal transverse colon, descending colon, rectum and anal canal to the pectinate line. It also forms much of the urogenital system.  The terminal portion of the hindgut is enlarged as the cloaca.  The cloaca develops into the rectum and upper 2/3 of the anal canal, while its anterior subdivision, the urogenital sinus, develops into the bladder and in the female, the urethra and vestibule, while in the male the prostatic urethra. 

During the rotation of the midgut, the descending colon is displaced to the left and is fixed in a retroperitoneal position (S-Figs. 13.27/14.27, 13.30/14.30). The sigmoid colon remains intraperitoneal in nature, but its mesentery is shortened during the fixation of the descending colon. The dorsal mesenteries of the rectum and anal canal disappear, as they become retroperitoneal organs. 

During the folding process, the ectoderm of the body wall ingresses toward the endoderm of the cloaca (S-Fig. 13.36/14.36). The ectodermal ingrowth is called the proctodeum or anal pit. The union of proctodeal ectoderm and cloacal endoderm, with no intervening mesoderm, is the cloacal membrane.

The cloaca is subdivided by a down growth of splanchnic mesoderm called the urorectal septum (Tourneux's fold) and two lateral bars of mesoderm or Rathke's folds (S-Fig. 13.36/14.36). As the cranial urorectal septum migrates downward, it meets the pair of folds that arise from the lateral walls.  These lateral folds grow sagittally to meet the descending urorectal septum near the cloacal membrane. When these folds interface with each other and the descending urogenital septum, they produce a complete division and separation of the cloaca into the urogenital sinus, rectum and the upper portion of the anal canal.  Thus, the upper portion of the urorectal septum is derived from the descending visceral mesoderm, while the caudal portion of this septum is formed by the lateral folds. Misalignment of the descending urogenital septum and lateral folds results in many of the abnormalities associated with the hindgut.

The urorectal septum joins the cloacal membrane and divides it into an anal membrane and a urogenital membrane.  The point where the urorectal septum intersects the cloacal membrane is the future site of the perineal body, which many clinicians call the perineum. The perineal body is an extremely important structure in obstetrics and gynecology, and its also important in the male.  It serves as the anchor point for many of the perineal muscles.  In the adult, it has a high content of elastic connective tissue and some smooth muscle.

 

II.  Anatomical Considerations  (see Table I)

The anal and urogenital membranes represent the points of separation of ectodermally and endodermally derived structures. When these membranes rupture, ectoderm and endoderm become continuous with each other.  In the UG triangle, the point of separation of ectodermally and endodermally derived structures is at fossa navicularis in male urethra and at the hymen in the distal vagina. The location of the cloacal membrane is approximated by the presence of the pectinate line in the distal 1/3 rd of the anal canal. . The anal valves are thought to be remnants of the cloacal membrane, while the anal columns appear to ascend from the pectinate line.  The anal columns are produced by the internal hemorrhoidal venous plexi, which is the normal distal venous drainage of the superior rectal vein (see Table I). 

Because the pectinate line represents the point where ectoderm and striated muscle derived from the cloacal myotome meets endoderm and visceral mesoderm from the hindgut, there is an abrupt change in the neurovascular supply (see Table I).

 

III.  CONGENITAL ABNORMALITIES OF THE HINDGUT

Anorectal abnormalities are the most common GI anomalies.  The abnormalities are subdivided into high and low depending on whether the bowel terminates above or below the puborectalis muscle (puborectal sling). 

A.  Urorectal Septal Defects  (S-Fig. 13.37/14.37)

1.   Failure of the lateral (Rathke) folds, which are inferior in position, result in failure of the inferior portion of the urorectal septum near the anal membrane to close. This produces rectourethral fistulas.  In males, these are rectoprostatic urethral fistulas.  In females, these are rectocloacal fistulas that involve the rectum, urethra and vagina or a rectovaginal or ano-vestibular (located at vaginal-cloacal junction) fistula.

2.  Failure of both urorectal septum (Tourneux) and lateral (Rathke) folds produces rectovesical fistula in males. In females, this could disrupt the fusion of the paramesonephric ducts producing paired bilateral vaginas and uteri that empty into the bladder.

3.  Malalignment of the folds results in urorectal fistula.  In males, a fistula is formed between the rectum and the prostatic urethra often accompanied by penile urethral stenosis.  Meconium is present in the urine.  In females, a rectovaginal fistula is formed.

B.  Low Anorectal Defects (Abnormalities involving the proctodeum, and anal pit that forms the distal 1/3rd of the anal canal and anus)

1.  Imperforate (abnormally closed) anus is either the failure of the anal portion of the cloacal membrane to rupture, or it ruptures incompletely.  The proctodeum fails to become continuous

 

Table I:  Anatomical Changes at the Pectinate Line

External to the Pectinate Line

Internal to  the Pectinate Line

Structures develop from ectoderm and myotomes.

Structures develop from endoderm and visceral mesoderm.

Muscles and epithelial covering are skeletal muscles and cutaneous structures.

Muscles and epithelial covering are smooth muscle and columnar and cuboidal epithelium.

Arteries are the inferior rectal branches of the internal pudendal artery.

Arteries are branches of the inferior mesenteric artery's superior rectal artery and internal iliac artery's middle rectal artery.

Venous drainage is to interior rectal v. to internal pudendal vein to internal iliac vein (systemic venous system)

Venous drainage is superior rectal v. to inferior mesenteric v. to portal system of veins

Innervation is the pudendal nerve with general somatic efferent, general somatic afferent, and postganglionic sympathetic fibers. Sensation of pain is highly localized.

Autonomic innervation: postganglionic sympathetics from inferior mesenteric ganglia that follow either the superior rectal artery or fibers that pass in the superior hypogastric and inferior hypogastric plexi. Parasympathetics preganglionic fibers are part of the pelvic splanchnics.  The ganglia are in the wall of the anal canal and rectum and they have very short postganglionic fibers.  Sensation from this visceral region is due to distension or contraction of the gut, as is the case for the rest of the gut

Lymphatics drain to the inguinal nodes

Lymphatics drain to the lumbar nodes associated with the inferior mesenteric artery

with the endoderm of the hindgut.  The rectum is not properly connected to the body wall.  It occurs in 1:5000 births and has a higher incidence in males. Anal stenosis is a narrowing due to partial rupture of the anal membrane, but the anus is located in the normal position.

2.  Anal agenesis (insufficient anus) occurs without fistula- rectum ends blindly, with location of anal pit sometimes marked by small dimple or pigmented spot. The anal canal ends blindly or there is an ectopic anus.  Anal agenesis occurs with fistula into the urethra or vulva and is due to the failure of urorectal septum to divide the cloaca.

3.  Covered anus (membranous atresia, anocutaneous occlusion) occurs when the anus is in the normal position but is covered by genital folds.  It is usually in males because the genital folds do not fuse in females.  If the anus is displaced anteriorly due to a defect in the perineal mesoderm then the condition is anocutaneous stenosis/ anterior anus.

C.  High Anorectal Defects

1. Anorectal agenesis, with or without fistula.  The rectum ends high with no lower rectum, anal canal or anus.  This is the most common type of defect.  Fistulas occur between the rectum and urethra or vagina depending on the sex.  Anorectal agenesis is probably due to a failure of the growth of both the proctodeum and urorectal septum. 

2. Rectal atresia  The anus and anal canal are normal, but the rectum ends blindly.  This is possibly due to a loss of blood supply.

3. Persistent cloaca (in females).  The bladder, vagina and rectum form one common cavity.  The end results of surgical correction are poor if the endorectal pull-through procedure does not take into account the presence of the puborectalis and external sphincter muscles.  These muscles are necessary for anal continence.  In addition, low abnormalities are associated with the formation of the internal anal sphincter, external anal sphincter and puborectalis muscle.  High anorectal defects such as anal or anorectal agenesis have a poor prognosis due to the loss of the future internal anal sphincter.  The external anal sphincter is hypoplastic and not functional.

D.  Congenital Aganglionic Megacolon (Hirschsprung's Disease) (see also S-p. 478)

Congenital aganglionic megacolon (Hirschsprung's disease) is due to the failure of neuroblast migration with no ganglion cells in affected Auerbach's or Meissner's plexi.  The child fails to pass meconium and the abdomen distends.  The condition always involves the rectum, but can also involve adjacent components of the gut (25% rectum; 50% sigmoid colon & 25% proximal bowel)  It was thought that it was due to an arrest of the craniocaudal migration of enteric innervation.  However, enteric innervation starts at both ends and proceeds toward the center.  The aganglionic bowel is the narrowed distal rectum or bowel.  The obstructed bowel is normal in diameter with the obstruction often being only incomplete.  The peristaltic wave brings the bowel contents to the aganglionic distal portion.  The normal proximal bowel enlarges (megacolon) just before the narrow abnormal bowel, which produces the blockage.

Full thickness rectal biopsy demonstrates the absence of ganglion cells.  Acetylcholinesterase histochemistry is now used as a marker for these parasympathetic ganglion cells.  Repair includes relief of intestinal obstruction by a colostomy to the right half of the transverse colon.  The fistula is repaired and a pull through procedure at the level of the puborectal sling anastomoses the rectum - anal canal and anus.

Inspection of the perineum is part of the routine examination of a newborn child.  The anorectal deficit should be identified soon after birth.  If the anus or anal canal is absent and a fistula is present, then meconium should be noted in urine or at the vaginal opening.

 

STUDY QUESTIONS (Note: Some questions are best answered after reading the Urinary System chapter)

 

What does the hindgut gives rise to and which parts are retroperitoneal?

Embryologically speaking, what makes the pectinate line an important demarcation?  How does the embryology explain the anatomical differences in the vascular supply, lymphatic drainage, and innervation in this region?

 

Hindgut abnormalities are associated with the malformation of the urorectal septum as well as the urovaginal septum in females.  What are the abnormalities associated with the partitioning of the cloaca and what are the consequences of each?  Where do fistulas from the anus or rectum commonly end up in males and females.

What is imperforate anus?

What other types of abnormalities can affect the rectum and anus?

 

What causes Hirschsprung's disease (aganglionic megacolon)?  Where does the bowel become distended and why?