DEVELOPMENT OF THE GASTROINTESTINAL SYSTEM

Foregut and Midgut

by Bruce I. Bogart, Ph.D.

 

Objectives

I INTRODUCTION
A. Peritoneum
B. The Trilaminar Embryo
C. Folding of the Trilaminar Embryo
D. Partitioning of the Intraembryonic Coelomic Cavity
E. Oropharyngeal and Cloacal Membranes

II. DEVELOPMENT OF THE CAUDAL FOREGUT
A. Formation of the Liver
B. Rotation of the Stomach and Formation of the Lesser Sac
C. The Lesser Sac
D. Formation of the Peritoneal Ligaments from the Dorsal Mesogastrium
E. Development of the Pancreas

III. DEVELOPMENT OF THE MIDGUT
A. Physiological Herniation
B. Reduction
C. Fixation

IV. CONGENITAL ABNORMALITIES OF THE FOREGUT AND MIDGUT
A. Congenital Anomalies of the Lower Respiratory System
B. Congenital Anomalies of the Diaphragm
C. Congenital Anomalies of the Caudal Foregut
D. Defects of Aberrant Folding or Reduction
E. Congenital Abnormalities of the Midgut

STUDY QUESTIONS

 

 

NOTE:  Figures referred to are from Netter (N), Grant's Dissector (G), Sadler (S) or original drawings reproduced in the text.


Objectives

1.  To describe the derivatives of the three portions of the gut tube, the development of the peritoneal cavity and the diaphragm, and the consequences of abnormal development.

2.  To understand the details of the process of rotation of the foregut and midgut that gives rise to adult relationships and the abnormalities associated with these processes.

3.  To learn about the partitioning of the hindgut and associated abnormalities.

 

I INTRODUCTION

A.  Peritoneum 

The abdominal cavity is lined by a continuous serous membrane called the peritoneum (Grants G-106-111).  The peritoneum has two components: a visceral peritoneum in intimate contact with the viscera and a parietal peritoneum in contact with the body wall.  Recall that the embryonic lateral mesoderm divides into visceral (splanchnic) and somatic (parietal) mesoderm.  The visceral peritoneum is derived from the visceral mesoderm, while the parietal (somatic) peritoneum is derived from the somatic mesoderm.  The peritoneal cavity is the potential space between the two layers of peritoneum containing small amounts of serous fluid.  No organs are within the peritoneal cavity.  The peritoneal cavity is closed in males and opened in females by means of the uterine tubes.

Intraperitoneal organs are those organs that are surrounded and suspended by visceral peritoneum, The peritoneal ligaments are also derived from visceral mesoderm and are therefore classified as visceral peritoneum. 

Retroperitoneal organs are those organs, which may have peritoneum on one or more sides, but are not suspended by peritoneum. These retroperitoneal organs are usually embedded in subserous fascia in the body wall. Retroperitoneal organs may initially develop in a retroperitoneal position or they may initially develop as intraperitoneal organs that become retroperitoneal due to a process referred to as fixation. These organs are often referred to as secondarily retroperitoneal organs.

Peritoneal reflections are the points where the parietal and visceral peritonea are continuous. At these points, the peritoneum extends from the body wall to the organ it will surround. The peritoneum extending from the body wall to the organ is considered visceral peritoneum.  Double layers of visceral peritoneum are called peritoneal ligaments.  These ligaments may contain neurovascular bundles from the body wall to the intraperitoneal organs.  Mesenteries are double layers of visceral peritoneum that "sling" the intestine from the posterior abdominal walls.  Mesenteries often contain neurovascular bundles.  An example is the mesentery, which suspends the jejunum and ileum from the posterior wall and contains intestinal branches of the superior mesenteric artery and vein as well as autonomic nerves and lymphatics that run with the superior mesenteric vessels.

B.  The Trilaminar Embryo

The trilaminar embryo consists of ectoderm, mesoderm and endoderm. The ectoderm faces the amniotic cavity.  The endoderm lines the yolk sac and the mesoderm is found between the ectoderm and endoderm.  The mesoderm divides into three components: paraxial, intermediate, and lateral mesoderm (lateral plate) (Fig. 5.9/6.7).  The lateral mesoderm divides into somatic (parietal) and visceral (splanchnic) mesodermal layers (Fig. 5.13/6.12).  The division of the lateral mesoderm into two components is a key step in the development of the intraembryonic coelomic cavity, which is eventually subdivided into the future pericardial, pleural and peritoneal cavities.

In the middle and caudal portions of the embryo, the division of lateral mesoderm is clear with the somatic mesoderm in contact with the ectoderm and the visceral mesoderm with the endoderm.  The somatic mesoderm is in contact with the ectoderm to form the somatopleure, which forms parts of the body wall (skin, dermis, parietal serous membranes, muscles and bones).  The visceral mesoderm and adjacent endoderm forms the splanchnopleure, which forms the visceral serous membranes, gut tube and associated glands.  The intraembryonic coelomic cavity is found between the two layers of mesoderm (Fig. 10.1/11.1).

Simultaneously, in the rostral (cranial) portion of the embryo, small vesicles coalesce to form cavities within the mesoderm.  The cavities will further coalesce to form a single intraembryonic coelomic cavity that is now continuous with the intraembryonic coelomic cavity described above.  The rostral intraembryonic coelomic cavity is in the shape of an inverted "U" with (1) the inverted end of the U in the most rostral portion of the embryo, and (2) it is associated with the cardiogenic region.  Indeed, the closed end of the U is the future pericardial cavity and the limbs of the U become the pleural and peritoneal cavities. 

C.  Folding of the Trilaminar Embryo

Folding of the flat trilaminar embryo results in the following:  (1) the formation of the embryonic body,  (2) partitioning of the continuous intraembryonic coelomic cavity into pleural, pericardial and peritoneal cavities, and (3) formation of the gut tube.

The formation of the gut tube and the partitioning of the serous cavities occur simultaneously.  Folding takes place in both the cranial-caudal (logitudinal) and lateral (trans­verse) planes.  During the longitudinal folding, the head and tail of the embryo rotate 180o.  Two landmarks can be used to follow this rotation.  The cranial landmark is the septum transversum; the caudal landmark is the allantois (Fig. 5.16/6.16).  The septum transversum is a mesodermal mass that lies rostral (toward the beak) to the future heart tube and intraembryonic coelomic cavity.  As the nervous system develops, the septum transversum, future pericardium, and heart tube flex 90o.  During this process, the septum transversum moves ventral to the developing heart tube.  Upon further folding the septum transversum will come to lie caudal to the heart tube.  The septum transversum will become the diaphragm's central tendon, which incompletely separates the pericardial cavity from the peritoneal cavity.  This 180o of flexion also results in the yolk sac endoderm being folded into the embryo to help form the foregut portion of the gut-tube (Sadler S-Fig. 13.1/14.1).  Caudally, the connecting stalk, which contains the allantois, moves 180o to help form the caudal ventral wall and the umbilical cord.  At the same time, the yolk sac endoderm is folded into the embryo to form the hindgut portion of the gut-tube.

Lateral folding helps complete the ventral body wall.  Here the growth of the amnionic sac may play a role in the movement of the somatopleure first laterally and then anteriorly.  Early in development, lateral folding brings the two limbs of the early intraembryonic coelomic cavity together to form a single peritoneal cavity below the level of the foregut (S-Fig. 13.2/14.2).  Lateral folding also completely closes the ventral wall except in the region of the midgut where the yolk stalk is initially retained and the umbilical cord is formed. 

D.  Partitioning of the Intraembryonic Coelomic Cavity

Cranial folding results in a large pericardial cavity situated ventral to the cranial foregut.  The pericardial cavity communicates with the developing peritoneal cavity by means of the two limbs of the original inverted U shaped intraembryonic coelomic cavity.  These limbs, which are now identified as the pericardioperitoneal canals, pass posterior to the septum transversum and along side of the foregut tube.  The lung buds develop after the heart (S-Fig. 10.4/11.6).  The lung buds begin to grow into the pericardial cavity with the splanchnic mesoderm producing the visceral serous membrane, future visceral pleural membranes on their surfaces.  As the developing lung grows laterally and anteriorly, the adjacent parietal mesoderm responds by producing folds called the pleuropericardial folds.  These folds contain the phrenic nerves and common cardinal veins.  As the lungs continue to grow, the pleuropericardial folds migrate into the pericardial cavity to reach the primitive mediastinum and the root of the lung (S-Fig. 10.5/11.7). The pleuropericardial folds separate (partition) the pericardial cavity from the two pleural cavities.  This partitioning process also accounts for the additional connective tissue layer that is found on the external surface of the serous parietal pericardium, the very tough fibrous parietal pericardium.  In addition, the two phrenic nerves migrate from the body wall into the thoracic cavity.  Here, they lie in the plane of the fibrous parietal pericardium.  The right common cardinal vein along with the right anterior cardinal vein form the superior vena cava, while the left common cardinal vein regresses forming only the distal segment of the coronary sinus and the oblique vein.

The newly formed pleural cavities still communicate with the peritoneal cavity by means of the pleuroperitoneal canals.  These canals are closed by pleuroperitoneal folds, which are formed by a delamination of the posterolateral body wall (S-Fig. 10.6/11.8).  This excavation of the posterolateral body wall also accounts for the formation of the pleural cavity's costodiaphragmatic recess.  The pleuroperitoneal membranes contribute to the formation of the diaphragm along with the septum transversum, mesoesophagus, and myoblasts that migrate in from the lower thoracic body wall.  All of the myoblasts, which will become the diaphragm's skeletal muscle, are innervated by the phrenic nerves.  Sensory innervation of most of the diaphragm is from the phrenic nerves, except for the posterolateral margins, whose sensory fibers come from the lower intercostal nerves.

E.  Oropharyngeal and Cloacal Membranes

There are some places where ectoderm and endoderm come into direct contact without intervening mesoderm. This happens caudally at the cloacal membrane and cranially at the oropharyngeal (buccopharyngeal) membrane. The oropharyngeal membrane ruptures early.  This may be due to the absence of the mesoderm and subsequent lack of development of blood vessels.  The rupture forms the superior opening of the gut tube, allowing amniotic fluid into the gut tube. Later, the cloacal membrane is subdivided into anal and urogenital membranes, which also rupture.  In the adult, regions such as the tongue's sulcus terminalis and the anal canal's pectinate line are very interesting, since they mark points where ectodermal and endodermal structures meet.  At these landmarks, one side of the GI tract is supplied by the somatic neurovascular bundles associated with the somatopleure, while the other side is by the visceral neurovascular bundles associated with the splanchnopleure.

F.  Arterial Supply to the Foregut, the Midgut and Hindgut

The parts of the future abdominopelvic gut are the caudal end of the foregut, the midgut and hindgut.  Each segment of the gut, starting with the caudal foregut, midgut and hindgut, is supplied by a single major artery (Figure 1).  These arteries also supply the organs that develop from that part of the gut (S-Fig. 13.4/14.4). 

The celiac artery supplies the caudal foregut, which gives rise to the esophagus, stomach, duodenum to the duodenal papilla, pancreas, biliary ducts, gall bladder, and liver. 

The superior mesenteric artery supplies midgut organs. The midgut organs include the remainder of the duodenum, ileum, cecum, ascending colon, and proximal half to two-thirds of the transverse colon. 

The inferior mesenteric artery supplies the hindgut organs. They are the remainder of the transverse colon, descending colon, sigmoid colon, rectum and anal canal to the pectinate line. 

Transitional regions are supplied by two of the above arteries. Anatomically, the foregut is continuous with the midgut just distal to the duodenal papilla (the common opening for both the common bile duct and pancreatic duct into the duodenum).  The midgut is continuous with the hindgut approximately where the proximal half to two-thirds of the transverse colon meets the remaining distal portion of the transverse colon (S-Fig. 13.4/14.4).  The hindgut is continuous with the somatic portion of the anal canal at the pectinate line.

 

Figure 1

1- PERITONEUM

6- FUTURE GREATER OMENTUM

2- FUTURE GASTROSPLENIC LIGAMENT

7- FUTURE LESSER OMENTUM

3 SUPERIOR MESENTERIC ARTERY

8-CELIAC TRUNK

4 INFERIOR MESENTERIC ARTERY

1' UMBILICAL VEIN

5 FALCIFORM LIGAMENT

2' VITELLINE ARTERY

 

These transitional points represent regions of collateral circulation that can be identified by knowledge of the development of the gut.  The foregut-midgut collateral circulation occurs just distal to the duodenal papilla, where the superior pancreaticoduodenal arteries, which arise from the celiac trunk branches anastomose with inferior pancreaticoduodenal arteries, which arise from the superior mesenteric artery (N 291).  The midgut-hindgut collateral circulation occurs across the transverse colon. Here, the superior mesenteric artery's middle colic branch anastomoses with the inferior mesenteric artery's left colic branch to form the marginal artery (of Drummond) (N 296).  The visceral-somatic collateral circulation takes place across the anal canal's pectinate line where the inferior mesenteric artery's superior rectal branch anastomoses with the pudendal artery's inferior rectal artery.  The superior rectal artery also anastomoses with the internal iliac artery's middle rectal branch.

 

II.  DEVELOPMENT OF THE CAUDAL FOREGUT

A.  Formation of the Liver

The gut begins as a simple tube suspended from the posterior wall by the primitive dorsal mesentery.  Initially, a swelling of the caudal foregut develops into the future stomach (S-Fig. 13.5/14.5).  The stomach's ventral surface, which will become the lesser curvature, grows slower than stomach's dorsal surface, which will become the greater curvature (S-Fig. 13.8/14.8).  At the same time, a cord of endoderm and adjacent visceral mesoderm starts just distal to the developing stomach and grows into the septum transversum (S-Figs. 13.14/14.14, 13.15/14.15).  This outgrowth of cords of endoderm and mesoderm is the liver bud, which becomes the biliary duct system, gallbladder, and liver.  The ventral pancreatic bud is an outgrowth of the gut that originates very close to the origin of the liver bud, while just proximal to the origin of the liver bud another outgrowth occurs that is the dorsal pancreatic bud. 

The liver begins developing in the septum transversum (S-Fig. 13.14/14.14). It quickly outgrows the septum transversum extending caudally into the peritoneal cavity.  However, it retains an association with the developing diaphragm that becomes the bare area of the liver in the adult. Here, the liver comes into contact with the fascia of the inferior surface of the diaphragm.  As the liver overgrows the diaphragm, it grows into the ventral mesentery (S-Fig. 13.15/14.15).  There is no mesentery ventral to the developing gut below the level of the foregut, i.e., the midgut and hindgut do not have a ventral mesentery.  The liver now occupies the ventral mesentery that lies between the fetus' ventral wall and the stomach.  The mesentery posterior to the gut is the dorsal mesentery.  The stomach's dorsal mesentery is referred to as the dorsal mesogastrium.

All of the peritoneal ligaments associated with the liver and the stomach's lesser curvature are derived from the ventral mesentery.  The falciform ligament is the portion of the ventral mesentery between the ventral wall and the liver since it is sickle shaped (Fig. 13.15/14.15). The lesser omentum stretches between the liver and the stomach and first portion of the duodenum.  It can also be subdivided into the hepatogastric ligament, which stretches between the liver and the lesser curvature, and the hepatoduodenal ligament, which stretches between the liver and the duodenum.  The liver's coronary ligament is the peritoneal reflections from the diaphragm to the liver that is found at the margins of the liver's bare area.  Peritoneal ligaments typically have two contiguous layers.  However, the coronary ligament is unusual in that the bare area separates its two layers of peritoneum from each other so the coronary ligament's superior and inferior layers have separate sites of reflection.  However, the two layers do come together in the typical manner in the formation of the right and left triangular ligaments, the falciform ligament, and the lesser omentum. 

Unlike the liver, the spleen is not an outgrowth of the foregut.  It develops coincidentally with the gut in the dorsal mesogastrium, but independently of the gut.  However, its splenic artery is a branch from the celiac trunk. 

B.  Rotation of the Stomach and Formation of the Lesser Sac

The stomach primordium enlarges and broadens in the anterior-posterior plane. As stated above, the dorsal border of the stomach grows faster than the ventral one (S-Fig. 13.8/14.8). This differential growth produces the greater and lesser curvatures of the stomach (G-112). The formation of the lesser sac can be accounted for by several phenomena that occur simultaneously. 

At the level of the caudal foregut, the peritoneal cavity is subdivided into a right and left component by the dorsal and ventral mesenteries of the stomach (Figure 1).  That is not true for the midgut and hindgut since they lack a ventral mesentery.  The peritoneal cavity becomes partially divided into the greater sac and the lesser sac, which is behind the stomach.  These two subdivisions communicate by means of the epiploic foramen of Winslow. Active excavation of the dorsal mesogastrium and rotation results in the development of the lesser sac. The primitive dorsal mesogastrium is relatively thick compared to the ventral mesentery.  On its right side, little vacuoles form and coalesce to form a single cavity that expands transversely and superiorly within the stomach's dorsal mesogastrium and to the right of the esophagus (S-Fig. 13.9/14.9).  This cavity is the future lesser sac (omental bursa).  The developing diaphragm and the liver cut off the uppermost part of the developing lesser sac. 

Rotation of the stomach with a concurrent rearrangement of its mesenteries is the second step in this process.  The liver, stomach, spleen, aorta, and the visceral peritoneum forming the ligaments are initially found in the midline (Figs. 1 & 2).  The stomach undergoes a 90o clockwise rotation to the right through its longitudinal axis (Figs. 3, 4, & 5).  This results in the liver, ventral mesentery, and lesser curvature of the stomach moving to the right.  As the right side of the stomach becomes its dorsal surface, the right vagus will now be located on the posterior aspect of the lesser curvature of the stomach and attached esophagus.  The stomach's greater curvature, spleen, and dorsal mesentery (the future greater omentum) will move to the left.  As rotation results in the stomach's left side becoming its ventral surface, the left vagus is now located on the anterior surface of the lesser curvature and the attached esophagus. 

Due to the differential growth of the greater curvature and 90 0 rotation, the stomach's axis shifts from a longitudinal (sagittal) plane (Fig. 2) to a coronal plane (Fig. 4).  The second rotation takes place in the coronal plane (S-Figs. 13.10/14.10, 13.11/14.11).  The distal end of the foregut, which is the pylorus and proximal duodenum, rotates from its caudal position to a position superior and to the right.  This rotation brings the pylorus and adjacent duodenum into close proximity to the liver.  In the adult, these organs make impressions on the liver's visceral surface.  This narrowing of space between the pylorus and liver contributes to the formation of the epiploic foramen of Winslow.

C.  The Lesser Sac

The lesser sac (omental bursa) (G-108, 109, Figures 3, 4 & 5) has an upper recess found anterior to the caudate lobe of the liver and a lower recess between the layers of the greater omentum (omentum, L. - fatty skin).

The boundaries of the lesser sac are

1) the lesser omentum,

2. the visceral peritoneum over the stomach,

3) the greater omentum,

4) the parietal peritoneum over the posterior abdominal wall and diaphragm,

5) the posterior leaf of the coronary ligament,

6) on the left, the splenorenal and gastrosplenic ligaments,

7) on the right, the epiploic foramen (of Winslow).

The epiploic foramen of Winslow (epiploon is from Greek for omentum) is the site of communication between the lesser sac and the remainder of the peritoneal cavity or the greater sac. Its boundaries are:

1) anteriorly, the hepatoduodenal ligament,

2) posteriorly, the peritoneum over the inferior vena cava & right crus of the diaphragm,

3) superiorly, the peritoneum over the caudate lobe of the liver,

4) inferiorly, the peritoneum over the duodenum & the reflection of the hepatoduodenal ligament.. 

The peritoneum is reflected over the duodenum to help form the hepatoduodenal ligament.  This point is the right gastropancreatic fold and this is the point where the portal vein, proper hepatic artery and common bile duct enter the hepatoduodenal ligament.  It is important to remember that the peritoneal cavity is considered one unit that is subdivided into the greater and lesser sacs. 

D.  Formation of the Peritoneal Ligaments from the Dorsal Mesogastrium

The differential growth of the dorsal border of the stomach is accompanied by a simulta­neous growth of the dorsal mesogastrium (S-Fig. 13.11/14.11).  The presence of the spleen is used to subdivide the continuous dorsal mesogastrium into the splenorenal and gastrosplenic ligaments (Figures 2-4).  Upon extensive growth, the inferior portion of the dorsal mesogastrium becomes the greater omentum.  However, since they are all subdivisions of the dorsal mesogastrium, they are continuous with each other.  This allows the splenic artery to run from the posterior wall through one ligament (the splenorenal ligament) to reach the spleen and then continue through a continu­ous ligament (the gastrosplenic ligament) to reach the fundus or through the anterior layers of the greater omentum to reach the right side of the stomach's greater curvature (Fig. 5).

The greater omentum (G-106, # 6; Figure 1) attaches the greater curvature of the stomach to the posterior abdominal wall (S-Figs. 13.12/14.12,13.13/14.13).  As the stomach's greater curvature develops, the adjacent greater omentum also grows to accommodate this differential growth and coronal rotation (Figure 7a).  Consequently, the greater omentum folds upon itself producing a four-layered peritoneal structure with two anterior and two posterior layers (Figure 7). The lesser sac's inferior recess is found between the greater omentum's anterior and posterior layers (G109, Figure 7a).  After birth, these four layers are usually fused inferiorly .  The anterior two layers contain the gastroepiploic arteries and veins (which are found close to the stomach's greater curvature and are branches of the splenic vessels found in the splenorenal ligament and the gastroduodenal vessels).  In addition, following the concurrent midgut rotation, the transverse mesocolon will fuse with the greater omentum's two posterior layers (see Figures 7b & 7c).

 

Figure 2  Before the 90 0 rotation of the stomach

 

The splenorenal ligament (G-109,  Figure 2 #5 and Figure 3) was originally in the midline of the embryo.  It migrates anterior to the left kidney during the 90o rotation of the stomach.  This ligament carries the splenic artery and vein to the spleen.  The tail of the developing pancreas extends into this ligament to reach the hilum of the spleen.

The gastrosplenic ligament (G-109, Figs. 3 & 4) is the portion of the dorsal mesogastrium that connects the spleen and the superior portion of the greater curvature of the stomach. It contains the short gastric vessels and left gastroepiploic vessels (branches of the splenic artery and vein).

 

Figure 3  900 Rotation of Stomach

Figure 4  Greater and Lesser Sacs of the Peritoneal Cavity

E.  Development of the Pancreas

The ventral pancreatic bud arises in close proximity to the site of origin of the liver bud (S-Fig. 13.21/14.21).  The proximal portion of the endodermal cord of cells becomes the common bile duct, which joins the ventral pancreatic duct to form the duodenal ampulla (of Vater).  The duo­denal ampulla typically is the duct formed by the main pancreatic duct and common bile duct.

The ventral pancreatic bud is carried dorsally and to the right into the dorsal mesogastrium by the rotation of the adjacent stomach (S-Fig. 13.23/14.23).  It is carried inferior to the dorsal pancreatic bud, which forms the superior portion of the head, neck, body, and tail of the pancreas.  The ventral pancreas, which forms the inferior portion of the head and the uncinate process, has a separate duct.  The ducts of the ventral and dorsal pancreas join.  The ventral pancreatic duct becomes the main passageway for secretion for both the inferior pancreatic head and its body and tail derived from the dorsal pancreatic bud.  Often an accessory pancreatic duct remains as a remnant of the proximal portion of the dorsal pancreatic duct.  It will always enter the duodenum proximal to the duodenal papilla.  This papilla is the nipple-like elevation that marks the entrance of the duodenal ampulla.

Figure 5  Lesser Sac

 

III.  DEVELOPMENT OF THE MIDGUT   

The midgut ( Figure 6) forms most of the small intestine (except the duodenum proximal to the bile duct), cecum, appendix, ascending colon, and the proximal 1/2 of the transverse colon.  The superior mesenteric artery is the blood supply to the midgut. The midgut is arranged as a loop of bowel whose axis is the superior mesenteric artery. The midgut is still attached to the yolk sac by the yolk (vitelline) stalk or duct (S-Fig. 13.5/14.5).  The midgut is suspended only by a dorsal mesentery.  It has no ventral mesentery.  The midgut's neurovascular bundles communicate with the body wall through the dorsal mesentery (S-Figs. 13.3/14.3, 13.4/14.4).

This superior mesenteric artery (viewed from the anterior abdominal wall) serves as the axis of rotation for the rotation of the midgut (S-Fig. 13.25/14.25).  Rotation takes place around the superior mesenteric artery, which divides the gut loop into cranial and caudal portions. When completed, the midgut is rotated 270 degrees counter-clockwise. For orientation purposes, the face of a clock is applied in the coronal plane with the center of the clock at the superior mesenteric artery,

In order to follow rotation, we can use the cranial and caudal limbs of the midgut loop as landmarks. The cranial limb gives rise to the duodenum distal to the duodenal papilla, the jejunum, and most of the ileum, the caudal limb differentiates into a small remaining part of the ileum, the cecum, the ascending colon and approximately the proximal half to two thirds of the transverse colon (S-Fig. 13.25/14.25).

There are three distinct stages in the rotation of the midgut: (1) physiologic (normal) herniation, (2) physiologic reduction of the hernia, and (3) fixation. During each step there is a certain amount of rotation and mobilization of the intestinal tract (see Figure 6).

A.  Physiological Herniation

A hernia is a protrusion or movement of an organ from its normal anatomical position, usually through the body wall (S-Fig. 13.26/14.26).  Due to differential growth of several organs which includes the kidneys, the liver and most importantly the cranial limb of the midgut elongating faster than the caudal limb, the midgut herniates through the umbilical opening into the umbilical cord (Figure 6a).  This herniation begins in the 6th week and is accompanied by a 90 counterclockwise rotation as viewed from the anterior surface of the fetus.  The plane of rotation is through the superior mesenteric artery.  The very rapid growth of the cranial limb drives it to the right of the superior mesenteric artery and the caudal limb moves to the left of the artery (Figure 6b)( Figs. 13.24/14.24, 13.25/14.25, 13.26/14.26).

B.  Reduction

Physiologic reduction of a hernia is the return of an organ(s) back into its proper anatomical position.  The abdominal cavity enlarges sufficiently to accommodate the midgut, which re-enters the abdominal cavity in a specific manner.  The proximal part of the cranial loop reenters the abdominal cavity first by passing beneath the superior mesenteric artery (the axis of rotation) and it now lies to the left of both the superior mesenteric artery and midline.  As reduction continues, the caudal limb enters second by passing above the superior mesenteric artery (Figure 6 c & d).

 

Figure 6 Different Stages of Midgut Rotation

Occurring first, the reduction of the cranial limb is accompanied by another 90o counterclockwise rotation.  After passing under the axis of rotation (superior mesenteric artery), the cranial limb now is found inferior to the artery.  Occurring second, the reduction of the caudal limb is also accompanied by a third 90o counterclockwise rotation (see Figure 6c & d). After passing over the axis of rotation, the caudal limb now lies superior to the superior mesenteric artery.  At the end of this stage of the midgut rotation, the proximal end of the caudal loop, which differentiates into the cecum and proximal colon, is located in the upper right quadrant of the abdomen in a subhepatic position and has undergone a total rotation of 270o.

The cecum and appendix are derived from the cecal diverticulum, which appears on the antimesenteric side of the caudal midgut loop (S-Fig. 13.28/14.28).  The walls of the cecum grow unevenly with a differential growth process producing the appendix at the distal end of the diverticulum. The appendix rapidly increases in length so that it is relatively long at birth.

C.  Fixation

Before fixation, all of the midgut is intraperitoneal and very mobile. Fixation is the process by which certain intraperitoneal organs' mesenteries come into contact with the parietal peritoneum resulting in the loss of this peritoneum.  The involved organs are now firmly attached to the body wall (S-Fig. 13.30/14.30).  Before midgut fixation, the cecum descends from its subhepatic position to its typical position in the right lower quadrant (Figure 6 d & e).  After the descent of the cecum, the visceral peritoneum of the ascending and descending portions of the colon are now in direct contact to the parietal peritoneum of the posterior walls.

The caudal duodenum and pancreas also become fixed at this time. When the caudal foregut rotates from a sagittal plane to a coronal plane the duodenum and the pancreas and their mesentery come to lie up against the posterior abdominal wall, with the pancreas adjacent to the kidney on the left side (S-Fig. 13.17/14.17).  The visceral and parietal peritoneal layers then fuse (Figure 7b & 7c).  The fused peritoneum is lost. These organs are now held in place by their variable relationship with the extraperitoneal fascia.  However, these organs retain visceral peritoneum on the surfaces that faces the peritoneal cavity.  Such organs are no longer suspended by peritoneum and are now considered secondarily retroperitoneal organs.  The process of fixation stabilizes the gut to prevent a peristalsis driven twisting (volvulus) of part of the gut. 

During the late stages of midgut rotation (Figure 6e) the transverse colon is located just inferior to the stomach's greater curvature. The posterior layers of the greater omentum come into contact with the transverse mesocolon and they fuse (S-Fig. 13.13/14.13). 


Figure 7                   a                                           b                                        c

a) Extensive growth of greater omentum contributes to the development of the lesser sac's inferior recess.

b) Fixation results in the loss of both of the visceral peritoneum on the dorsal surface of the pancreas and duodenum as these organs become retroperitoneal organs.

c) The transverse mesocolon fuses with the posterior leaf of the greater omentum.  The anterior and posterior layers of the omentum also fuse, leaving only a small portion of the anterior layer of the greater omentum, referred to as the gastrocolic ligament as a potential surgical approach to the lesser sac.

From A synopsis of Clinical Anatomy, by J.E. Healey & W.D. Seybold, W.B. Saunders, 1969.

 


IV.  CONGENITAL ABNORMALITIES OF THE FOREGUT AND MIDGUT

A.  Congenital Anomalies of the Lower Respiratory System

The development of the lower respiratory system especially the trachea and foregut are entwined, so that abnormalities of the trachea affect the cranial foregut derivative, the esophagus, and vice versa.

Stenosis is a narrowing of the lumen of an organ.  Atresia is when the lumen is either completely blocked or is lost.  (Frequency of atresia in decreasing order is esophagus, duodenum, ileum, jejunum, rectum)  A fistula is an abnormal communication or passage between the lumens of two organs that are supposed to be segregated.  A fistula can also be defined as an abnormal passage to the surface of an organ.

1.  Tracheoesophageal fistula is the most common congenital abnormality of the trachea.  Incomplete fusion of the tracheoesophageal folds leaves a defect in the tracheoesophageal septum that leads to a communication (fistula) between the trachea and esophagus (S-Fig. 13.7/14.7).  We are not sure of the mechanism (see also Development of the Respiratory System chapter).

Tracheoesophageal fistula is usually associated with esophageal atresia.  There are four types of tracheoesophageal (TE) fistulae.

a.  The most frequent TE fistula is when the upper esophagus ends as a blind pouch (esophageal atresia) and the trachea is joined to the distal esophagus above the carina (S-Fig. 13.7A/14.7A). 

b.  The TE fistula is confined to one region (S-Fig. 13.7C/14.7C).

c.  The TE fistula involves the upper esophagus with a second TE fistula that involves the esophagus slightly lower, with esophageal atresia between the two fistulas (S-Fig. 13.7E/14.7E).

d.  The TE fistula is accompanied by esophageal atresia with the distal esophagus completely detached from the trachea or upper esophageus.  Under these conditions there is no air in the stomach; air is normally swallowed and appears in x-rays (S-Fig. 13.7D/14.7D).

Availability of ventilatory support and improved total parenteral (besides intestine) alimentation (providing nourishment by means other than GI tract, i.e., intravenous alimentation) decreases the morbidity rate.  The length of the esophagus determines the treatment.  If the esophagus is of adequate length, its ends are anastomosed.  If the atretic esophagus is short, the esophagus above and below the atresia can be stretched (lengthened) by means of balloons. 

Infants with TE fistula and esophageal atresia have respiratory distress.  Upon swallowing, milk and saliva fill the blind esophagus, are regurgitated and pass into the trachea.  The presence of this material in the trachea produces coughing, and difficulty breathing.  Gastric contents may reflux into the trachea when the TE fistula is arranged as in several of the cases described above. 

2.  Esophageal stenosis or narrowing can occur at any place, but most often in the distal 1/3.  The esophageal lumen is almost obliterated during development and requires recanalization at the end of the embryonic period .  In esophageal stenosis, recanalization is incomplete, producing a web like or greatly narrowed lumen.  During normal development, the esophagus usually lengthens. When this does not occur, the resulting short esophagus will develop with the stomach displaced superiorly through the esophageal hiatus.

Esophageal compression can occur when the right subclavian artery arises from the sixth aortic arch and passes in front of or behind the esophagus (vascular rings see Cardiovascular System chapter).

All conditions where the esophagus is atretic or stenotic during fetal development can lead to polydramnios (too much amniotic fluid).  The fetus begins swallowing amniotic fluid which can be absorbed by the intestine.  Fluid is also excreted by the kidneys (see Urinary System chapter).  If there is a blockade early in the GI tract, then less fluid will be absorbed and the balance between absorption and excretion of fluid lost.  Too much amniotic fluid can have adverse consequences for lung development and can cause compressive malformations as well (see Congenital Malformations chapter).

B.  Congenital Anomalies of the Diaphragm

These abnormalities result from an incomplete closure of the diaphragm. 

1.  Congenital Diaphragmatic Hernia.  The most common of these is the failure of the pleuroperitoneal membrane (usually on the left) to partition the pleural cavity from the peritoneal cavity (S-Fig. 10.7/11.9).  This produces a foramen of Bochdalek.  This is an opening in the posterolateral diaphragm on the left, since the right pleuroperitoneal membrane closes earlier.  When the intestines return to the abdominal cavity during rotation of the midgut, the abdominal cavity is too small to accommodate them.  The intestines can herniate through the foramen of Bochdalek into the left pleural cavity.  Here, the intestine reduces the space for and thereby retards the growth of the developing lung (ie, displacing the left lung).  At birth, the child has respiratory distress (impaired respiration) and usually a concave (scaphoid - boat shaped) abdomen.  The lung is hypoplastic and greatly reduced in size, but functional if aerated.  The herniating abdominal organs have to be reduced, the defect closed and finally the lung aerated.  In some cases, the lung can achieve normal size. 

2.  The sternocostal or retrosternal hernia occurs through the sternocostal hiatus (foramen of Morgagni).  This potential opening is between the xiphoid and adjacent costal origins of the diaphragm (N-176).  The superior epigastric vessels do not pass through this foramen, but are confined to the ventral wall.  However, intestine may herniate into the pericardial cavity, or less often the heart may herniate into the peritoneal cavity.

3.  Esophageal hiatal hernias are congenital when the esophageal hiatus is enlarged, thus allowing a portion of the adjacent stomach to herniate into the thorax. The present, but not established thinking is that the esophagus does not elongate at the appropriate time.  The esophageal hiatus develops around the upper stomach rather than the esophagus.  When the esophagus does descend, the hiatus is too large.  Sometimes the short esophagus does not descend and remains in the thorax.  An enlarged esophageal hiatus may predispose an individual to an acquired esophageal hiatal hernia in adulthood. 

4.  Eventration of the diaphragm occurs when 1/2 of the diaphragm is composed of fibrous tissue instead of muscle.  This is possibly because myoblasts didn't migrate into one of the pleuroperitoneal membranes.  The clinical picture of eventration appears similar to a diaphragmatic hernia, but with a thin membrane.  On the affected side, the diaphragm paradoxically rises into the thorax upon inspiration, with a concurrent displacement of abdominal organs under the attenuated sac-like diaphragm.  While not a hernia, the ballooning of one side of the diaphragm does create a space-occupying lesion at the expense of the lungs.

C.  Congenital Anomalies of the Caudal Foregut

1.  Congenital hypertrophic pyloric stenosis is a medical emergency that presents itself in about the 3rd week of infancy.  The incidence is 1:150 males and 1:750 females.  A marked thickening (hypertrophy) of the circular smooth muscle that forms the pylorus produces a concurrent narrowing of the lumen (stenosis) of the pyloric canal.  The child fails to thrive (ie, weight loss), accompanied by constipation and projectile vomiting.  The content of the vomitus is not stained by bile because this defect is located proximal to the duodenal papilla.  One treatment consists of a surgical longitudinal incision through the hypertrophied musculature.

2.  Duodenal Stenosis and Atresia.  The lumen of the duodenum is normally obliterated and recanalized during development.  The recanalization process includes vacuolation and degeneration of cells (S-Fig. 13.18/14.18).  Duodenal stenosis usually involves the horizontal and ascending portions.  In this case, the vomitus would be stained by bile.  Duodenal atresia is a more common defect and usually, but not always, occurs in the descending or horizontal portion distal to the region of the duodenal papilla.  It is most common distal to the duodenal papilla (second portion of duodenum).  The infant begins vomiting within hours of birth and the vomitus is usually bile stained.  The distended stomach and proximal duodenum usually distend the epigastric region.  The double bubble sign is seen on an X ray that demonstrates fluid and gas in the stomach and duodenum, forming a fluid level.  Duodenal atresia is usually associated with many other abnormalities including Down syndrome, premature birth, annular pancreas, cardiovascular abnormalities, anorectal malformations and polyhydramnios. 

3.  Annular pancreas occurs during rotation of the duodenum (S-Fig. 13.23/14.23). There are many possible explanations for annular pancreas.  In one such possibility, the tip of the ventral pancreas becomes fixed and does not rotate with the duodenum, but becomes bifid.  With growth and fusion of the bifid portions of the pancreatic bud, the pancreas surrounds the duodenum.  While rare, it can obstruct the duodenum. 

4.  Biliary atresia is a potentially life threatening condition. It is thought to occur due to a failure of canalization of the bile ducts.  Jaundice appears soon after birth, along with dark colored urine and clay colored stool (no bile salts).  Prior to 1975, extrahepatic biliary atresia was incompatible with life.  It was uniformly fatal except when there was a large enough proximal bile duct that could be joined to the intestine.  Subsequently, many improvements in pre and postoperative management of the child, including precise dissection of the bile duct remnants at the liver hilum, significantly improved these statistics.  For infants with intrahepatic biliary atresia, liver transplantation is the only option. 

D.  Defects of Aberrant Folding or Reduction

1.  Umbilical hernia occurs when the umbilical scar is weak.  Most of these hernias will be self-resolving as the abdominal cavity enlarges.

2.  Omphalocele (exomphalos) is due to the failure of the reduction of the midgut at the umbilicus or a failure of the lateral folding process in the middle of the embryo (S-Fig. 13.31/14.31).  The herniated gut is covered by a translucent membrane formed by both the amnion and peritoneum with an intervening, undifferentiated mesenchyme (Wharton's jelly) that produces a loose connective tissue.  The omphalocele may be due to the cranial-caudal and lateral folds failing to fuse, so that the umbilicus fails to completely close. 

Epigastric and low midline omphaloceles may result from the incomplete migration of the cranial or caudal folds.  The umbilical cord is always attached to the apex of the omphalocele with the umbilical arteries and vein present in its walls. 

Congenital epigastric hernias may be due to a failure of the lateral folds to fuse completely during the transverse folding process.  This defect is in the linea alba between the umbilicus and the xiphoid process, occurs in males with greater frequency and often contains the falciform ligament and greater omentum. 

3.  Gastroschisis (gas-tros' ki-sis) is a defect of the full thickness of the ventral wall.  It is usually above the umbilicus and to the right, but never at the umbilicus (S-Fig. 13.31/14.31).  Gastroschisis is thought to be the result of a weakening of the ventral wall due to the regression of the right umbilical vein.  This condition is more serious than an omphalocele because the intestine is exposed without a peritoneal sac to the amnionic fluid.  The bowel has a dark, thick, shortened and matted appearance.  This defect is repaired by skin flaps, which are referred to as a silo.

E.  Congenital Abnormalities of the Midgut

Many of the midgut abnormalities are due to a deviation in one of the stages of rotation or fixation.  These are malrotations or irregularities (anomalies) in rotation and fixation.

1. Omphalocele is due to the failure of the herniated gut to return to the abdomen (see above).  It may be due to a failure of the folding process to reduce the umbilicus.  Omphalocele is covered by the amnion of the umbilical cord.

2. Nonrotation occurs when the gut is reduced, but there is no further rotation, (loss of last 180 degrees of rotation).  The small intestine lies on the right and the cecum and appendix lie on the left (S-Fig. 13.33A).  If everything else is normal, then the nonrotation is asymptomatic.  It may become a diagnostic problem if diseases of the appendix or colon present in the left lower quadrant instead of the right lower quadrant.  Usually incomplete rotation has occurred; or the first 90o of rotation has occurred so that the small intestine is on right and the large bowel is on the left. 

3. Reverse rotation.  Reduction occurs in such a manner that the cranial limb is superior to the superior mesenteric artery and the caudal limb is inferior to the artery (S-Fig. 13.33B).  The last 180 degrees of rotation are clockwise instead of counterclockwise.  Upon fixation, the duodenum lies anterior to the superior mesenteric artery and the transverse colon posterior to the artery.  The duodenum is not retroperitoneal, while the transverse colon can be.  Under these conditions, the superior mesenteric artery may obstruct the larger transverse colon.

4. Mixed or malrotation.  The cranial limb rotates only the first 90 degrees to the right, while the caudal limb rotates only the last 180 degrees. The result of this uncoordinated rotation is that the duodenum is fixed on the right and the cecum lies in the left upper quadrant or close to the midline just below the pylorus.  Thick peritoneal bands  produce a partial or total obstruction when they pass from the left sided cecum to the 2nd portion of the duodenum.  This position may be accompanied by a very short root of the mesentery.  These are Ladd's transduodenal bands that produce a predilection for volvulus.

5.  Volvulus-(latin for twisting) occurs if fixation is incomplete.  In midgut volvulus, the intestines hangs from a free mesentery.  Upon peristalsis, the intestines can twist in such a manner to obstruct the bowel or strangle its blood supply.  Poor fixation may also account for parts of the bowel becoming incarcerated beneath the mesentery, including paraduodenal hernias just to the left of the duodenojejunal flexure. 

Other anomalies associated with fixation include; subhepatic cecum, retrocecal appendix, and mobile cecum.  These conditions are asymptomatic and are often important only in the advent of a disease state, which presents with an unusual physical position, i.e., subhepatic appendicitis presenting in the upper right upper quadrant instead of in the right lower quadrant. 

a. Mobile cecum is a failure in the fixation process to completely fix the cecum.  The cecum can now move around and therefore not be in its normal anatomical position-- or be subjected to volvulus.

b. Subhepatic cecum results from the failure of the cecum to descend.  The appendix is now in the right upper quadrant.  A diseased subhepatic cecum can exhibit symptoms similar to a diseased gall bladder or kidney.

 

c. Retrocecal appendix is the most common of the malrotation abnormalities (S-Fig. 13.29/14.29).  The appendix is thrown dorsal to the cecum as it descends.  The appendix becomes fixed in this position and can extend dorsal to the ascending colon all the way to the hepatic flexure. 

6.  Meckel's (ileal) diverticulum is due to the persistence of the yolk stalk (S-Fig. 13.32/14.32).  It is often the site of inflammation that mimics appendicitis or gastroenteritis.  Meckel's (ileal) diverticulum contains all the layers of the ileum and may contain gastric or pancreatic tissue.  It is always found on the antimesenteric surface of the ileum, close to the junction with the cecum.  This is the original site of the yolk (vitelline) duct.  It can remain patent as an umbilico-ileal fistula.  This is often symptomless.  When symptoms are present, they are attributed to hemorrhage with/without pain due to the corrosive effect of gastric acid on mucosa.

7. Intussusception is an invagination of the bowel.  The portion of the bowel that is invaginated is called the intussusceptum and the portion of the bowel that receives the bowel is called the intussuscipiens.  While not a malrotation, this condition is important because it produces an obstructed bowel.  The mesentery of the bowel becomes compressed.  The accompanying venous and arterial obstruction produces edema and even necrosis of the bowel.

8. Intestinal stenosis and atresia occur most often in the ileum and duodenum.  It is most common at the level of the duodenal papilla, then ileum, and jejunum.  It is due to a failure of the lumen to recanalize either partially or completely (S-Fig. 13.34/14.34).  The failure to recanalize may be due to an interruption in the blood supply or a fetal vascular accident (produced by fetal volvulus or adhesion of the peritoneum that interferes with the blood supply).  This condition can be experimentally duplicated in fetal dogs by ligating blood vessels to a portion of the intestine.

9. Duplications consist of either closed cysts or tubular duplications that communicate at either one or both ends.  They always lie on the mesenteric side of the intestine and share a common wall.  These may be due to recanalization that leaves a central core of cells, producing a septum and two lumina.

 


STUDY QUESTIONS 

 

How does the embryological origin of the major structures of the gut (i.e., stomach, duodenum, jejunum, ileum, colon, rectum, anus) explain the innervation and blood supply of each?

 

What structures are derived from the foregut?  The splanchnopleure? 

How does the greater omentum form?  Why is it attached to the greater curvature of the stomach?  What other structures change their anatomical position as a result of foregut rotation?

How does the liver form and where does it develop?  What other structures come from the hepatic diverticulum? 

What is annular pancreas and how can you explain this abnormality from the embryology?

 

What is a trachoesophageal fisula?  What are some of its forms?  What is the cause?

         What are some of the symptoms?

Stenoses and atresias are common along much of the GI tract.  They can affect the esophagus, pyloric portion of the stomach, duodenum, bile duct, duodenum, ileum, and rectum).  What would you expect some of the physical findings to be in each (passage of stools, projectile vomiting, stained or unstained vomitus, etc.)? What are some of the chief causes (at least 3)

There are now possibilities for treatment of biliary atresia.  What options are available for extrahepatic and intrahepatic forms?

 

What are some of the common abnormalities associated with the diaphragm?  What are the causes?  What are some of the consequences for the development of the lung?

Esophageal hiatal hernia may occur in adulthood (typically in older people) as well as neonatally.  What is it and what are the causes?

 

What is the difference between an omphalocele, an umbilical hernia, and gastroschisis?  Each has a different embryological origin.  Explain.

What is polyhydramnios and what is its cause?

Failure of the midgut to rotate appropriately often has no consequences for the newborn.  What sorts of problems may arise that can result in an obstruction?

 

What structures of the gut are considered retroperitoneal?

Several abnormalities of fixation can occur as well.  Which of these are mentioned in the handout?  Why might they be a problem?  Some are also related to the malrotation mentioned above.

What is Meckel's diverticulum?  What is it?

Duplications of the bowel are also common abnormalities.  What causes them?