crosses the midline at the level of the third lumbar vertebra; and the deep respiration and both can descend by several centimetres when
fourth part ascends to the left of the second lumbar vertebra, reaching moving from lying to standing (Schwartz et al 1994, Reiff et al 1999).
the transpyloric plane in the region of the lower border of the first The length of the normal adult kidney, measured along its long axis,
lumbar vertebra (see Fig. 59.11B). The duodenojejunal flexure com- is approximately 11.5 cm in men and 11.0 cm in women (Hale et al
monly sits at L1 (range lower T11 to upper L3) (Mirjalili et al 2012b). 2010); the left kidney is a few millimetres longer than the right (Cheong
et al 2007, Glodny et al 2009, Mirjalili et al 2012b). There is a small
Small intestine and its mesentery reduction in renal length beyond 50 years of age (Glodny et al 2009).
The small intestine mesentery runs obliquely in a line from a point just Each kidney is approximately 5–6 cm wide. Both its longitudinal and
to the left of the lower border of the first lumbar vertebra (in the transverse axes are slightly oblique, such that the upper pole of each
transpyloric plane) towards the right iliac fossa. kidney is nearer the midline and the hilum is more anterior than the
lateral surface. The centre of the hilum is approximately 5–6 cm from
Appendix
the midline.
The appendix is located in the right lower quadrant of the abdomen The lower pole of the normal right kidney may occasionally be felt
but is highly variable in its length and position. Studies analysing in thin individuals by bimanual palpation via the renal angle on full
barium enemas in supine adults have shown the position of appendix inspiration.
base is variably located and rarely precisely at McBurney’s point (a point
two-thirds of the way along a line joining the anterior superior iliac Ureter


spine to the umbilicus) (Ramsden et al 1993, Naraynsingh et al 2002). The ureter descends on either side from approximately the level of the
transpyloric plane, slightly lower on the right, about 5 cm from the
Liver
midline. Each passes downwards just medial to the tips of the transverse
At the end of normal tidal inspiration, the inferior border of the liver processes of the lumbar vertebrae. In the pelvic cavity, each ureter curves
extends along a line that passes from the right tenth costal cartilage in medially to enter the base of the bladder.
the mid-axillary line to the left fifth intercostal space/sixth rib in the
mid-clavicular line (see Fig. 59.11B). It may be palpable in healthy adults Abdominal aorta and branches
on deep inspiration. The superior border of the liver follows a line that The abdominal aorta begins at the level of the body of the twelfth
passes from the right fifth rib or intercostal space in the mid-clavicular thoracic vertebra near the midline. It descends and bifurcates at


1047
95
rETPAHC
Key references
approximately L4 (range lower L3 to lower L5), usually just to the left allows access to the peritoneum at a point where there is relatively little
of the midline and up to 3 cm caudal to the umbilicus (Mirjalili et al extraperitoneal fat. Additional working ports are inserted through the
2012b). The position of the aortic bifurcation is shifted slightly proxi- anterior abdominal wall, avoiding major vessels such as the inferior
mally with a greater degree of lumbar lordosis (Moussallem et al 2012). epigastric artery.
The pulsations of the aorta can be felt in a thin, supine individual by
Surgical incisions
pressing firmly in the midline backwards on to the lower lumbar spine.
An easily palpable aorta in an obese person should raise the suspicion Most surgical incisions are sited according to surgical imperatives rather
of an aneurysm. than anatomical constraints. Access to the peritoneal cavity is gained by
dividing or splitting muscles. Common approaches include the midline
unpaired visceral arteries incision through the relatively avascular linea alba, the transverse
The coeliac trunk arises from the aorta immediately after it enters the suprapubic (Pfannenstiel) incision for pelvic procedures, and, in infants
abdomen at T12; the superior mesenteric artery arises most commonly and children, the upper abdominal transverse incision. In recent years,
at L1, close to the transpyloric plane; and the inferior mesenteric artery progressively more abdominal surgery has been performed using
usually arises at L3 (Mirjalili et al 2012b). laparo scopic procedures (minimally invasive or ‘keyhole’ surgery).
renal arteries Intestinal stomas (ileostomy, colostomy)
The renal arteries most commonly arise from between lower L1 and When possible, intestinal stomas are usually formed through transrec-
upper L2, with the lower border of L1 (approximately, the transpyloric tus incisions. A cruciate incision is made in the anterior rectus sheath
plane) being most common on both sides (Mirjalili et al 2012b). and the muscle fibres are split, avoiding injury to the epigastric vessels.
This incision offers the advantage that fibres of rectus abdominis
Iliac arteries


support the stoma, providing a dynamic, contractile surround that
The surface projection of the common iliac artery corresponds to the tends to reduce the risk of herniation occurring around the stoma.
superior third of a broad line, which is slightly convex laterally, from
the aortic bifurcation (see above) to a point midway between the ante- Suprapubic catheterization
rior superior iliac spine and the pubic symphysis. The external iliac The urinary bladder may be accessed for short- or long-term catheteriza-
artery corresponds to the inferior two-thirds of this line. tion through the anterior abdominal wall. As the bladder fills, the upper
Inferior vena cava part of its dome comes to lie in the preperitoneal ‘space’ in the suprapu-
bic region, where it can be relatively easily accessed by a midline trans-
The inferior vena cava most commonly forms at L5 in the transtuber-
cutaneous puncture through the linea alba.
cular plane (range upper L4 to upper S1) approximately to the right of
the midline (Mirjalili et al 2012b). The inferior vena cava leaves the Endoscopic surgery
abdomen by traversing the diaphragm at the level of the eleventh tho-
Endoscopic surgery is a broad term that encompasses all types of
racic vertebra.
surgery that are performed using flexible or rigid fibreoptic endoscopes
inserted through natural body orifices or small surgical incisions. It
PELVIS overlaps with the field of minimally invasive surgery. The aim is to
minimize or eliminate external incisions and hasten the patient’s
The posterior superior iliac spines lie at the level of the second sacral recovery, whilst providing optimum treatment of the pathology with
segment (McGaugh et al 2007); some individuals have an overlying an acceptably low risk of complications. In the abdomen and pelvis,
sacral dimple. This palpable bony landmark corresponds approximately therefore, it includes therapeutic procedures performed using an endo-
to the termination of the dural sac (Senoglu et al 2013) and the middle scope inserted via the mouth (gastroscope or duodenoscope), anus
of the sacroiliac joint. The second dorsal sacral foramina lies approxi- (proctoscope, sigmoidoscope or colonoscope), urethra (cystoscope or


mately 2–3 cm medial to the posterior superior iliac spine on each side ureteroscope) or vagina, or via small surgical incisions in the anterior
at an angle of 45° (McGrath and Stringer 2011). The latter is potentially or posterior abdominal wall (laparoscope and other endoscopic
useful when localizing the branches of the dorsal sacral rami in the systems).
treatment of refractory sacroiliac pain. A refinement of the technique is natural orifice transluminal endo-
scopic surgery, in which abdominal operations are performed using an
Sciatic nerve
endoscope inserted through a natural orifice (e.g. mouth, anus, urethra)
The sciatic nerve leaves the pelvis approximately one-third of the and then through an incision in the viscus that has been entered (e.g.
way along a line between the posterior superior iliac spine and stomach, bladder, vagina). For example, pelvic and intra-abdominal
the ischial tuberosity and enters the thigh approximately half way contents can be accessed through the vagina via the recto-uterine pouch.
between the greater trochanter and ischial tuberosity (see Fig. 78.16) Hysterectomy, oophorectomy, pelvic organ prolapse repair and incon-
(Currin et al 2014). tinence surgery are commonly performed using transvaginal techniques.
Other surface landmarks for pelvic structures are described in This approach avoids the morbidity of abdominal incision but there
Chapter 78. are risks of sciatic, femoral and common fibular nerve injury from
prolonged surgery in the lithotomy position.
A further development of endoscopic minimally invasive surgery has
COMMON CLINICAL PROCEDURES
been the introduction of robotically assisted surgery, which allows the
surgeon to manipulate precision instruments from a console that is
Pneumoperitoneum for laparoscopy remote from the patient whilst viewing the operative field in three
A pneumoperitoneum is frequently established by accessing the perito- dimensions. The procedure is becoming increasingly common in
neal cavity just below the umbilicus. An incision through the linea alba prostatectomy.
KEY REFERENCES
Furness JB, Callaghan BP, Rivera LR et al 2014 The enteric nervous system Mirjalili SA, Stringer MD 2012 The need for an evidence-based reappraisal


and gastrointestinal innervation: integrated local and central control. of surface anatomy. Clin Anat 25:816–18.
Adv Exp Med Biol 817:39–71. This issue of Clinical Anatomy features several original articles
A comprehensive review of gastrointestinal innervation and the complexities reappraising surface anatomy of the trunk using cross-sectional CT imaging
of the enteric nervous system. in supine adults. These articles provide a more evidence-based approach to
key surface anatomy landmarks in the chest, abdomen and pelvis.
Loukas M, Klaassen Z, Merbs W et al 2010 A review of the thoracic splanch-
nic nerves and celiac ganglia. Clin Anat 23:512–22.
A critical review of the thoracic splanchnic nerves.


Abdomen and pelvis: overview and surface anatomy
1047.e1
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rETPAHC
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Azaïs H, Collinet P, Delmas V et al 2013 Uterosacral ligament and hypogas- Mirjalili SA, McFadden SL, Buckenham T et al 2012b A reappraisal of adult
tric nerve anatomical relationship. Application to deep endometriotic abdominal surface anatomy. Clin Anat 25:844–50.
nodules surgery. Gynecol Obstet Fertil 41:179–83. Mirjalili S, Hale S, Buckenham T et al 2012c A reappraisal of adult thoracic
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m-mode ultrasonography: methods, reproducibility, and normal values. Moussallem CD, Abou Hamad I, El-Yahchouchi CA et al 2012 Relationship
Chest 135:391–400. of the lumbar lordosis angle to the abdominal aortic bifurcation and
Brierley SM, Linden DR 2014 Neuroplasticity and dysfunction after gastro- inferior vena cava confluence levels. Clin Anat 25:866–71.
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Cheong B, Muthupillai R, Rubin MF et al 2007 Normal values for renal position of human lumbar sympathetic ganglia and rami communi-
length and volume as measured by magnetic resonance imaging. Clin J cantes. Clin Anat 16:108–13.
Am Soc Nephrol 2:38–45. Naraynsingh V, Ramdass MJ, Singh J et al 2002 McBurney’s point: are we
Currin SS, Mirjalili SA, Meikle G, Stringer MD 2014 Revisiting the surface missing it? Surg Radiol Anat 24:363–5.
anatomy of the sciatic nerve in the gluteal region. Clin Anat doi: Oh CS, Chung IH, Ji HJ et al 2004 Clinical implications of topographic
10.1002/ca.22449. anatomy on the ganglion impar. Anesthesiology 101:249–50.
Drumm BT, Koh SD, Andersson KE 2014 Calcium signalling in Cajal-like Paraskevas G, Tsitsopoulos P, Papaziogas B et al 2008 Variability in superior
interstitial cells of the lower urinary tract. Nat Rev Urol 11:555–64. hypogastric plexus morphology and its clinical applications: a cadaveric
Epstein J, Arora A, Ellis H 2004 Surface anatomy of the inferior epigastric study. Surg Radiol Anat 30:481–8.
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A comprehensive review of gastrointestinal innervation and the complexities
Reiff JE, Werner-Wasik M, Valicenti RK et al 1999 Changes in the size and
of the enteric nervous system.
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Glodny B, Unterholzner V, Taferner V et al 2009 Normal kidney size and its implications for block placement during total body irradiation. Int J
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patients. BMC Urol 9:1–19. Roggin KK, Posner MC 2012 Modern treatment of gastric gastrointestinal
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A critical review of the thoracic splanchnic nerves. adults. Surg Radiol Anat 35:579–84.
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of surface anatomy. Clin Anat 25:816–18. 27:254–60.
This issue of Clinical Anatomy features several original articles
Zhang XM, Zhao QH, Zeng NL et al 2006 The celiac ganglia: anatomic study reappraising surface anatomy of the trunk using cross-sectional CT imaging
using MRI in cadavers. Am J Roentgenol 186:1520–3.
in supine adults. These articles provide a more evidence-based approach to
key surface anatomy landmarks in the chest, abdomen and pelvis.


CHAPTER Development of the peritoneal cavity,
60
gastrointestinal tract and its adnexae
muscularis mucosa, the connective tissue of the submucosa, the mus
POSTPHARYNGEAL FOREGUT
cularis externa and the external connective tissue are all derived from
the splanchnopleuric mesenchyme. The outer peritoneal epithelium is
The primitive gut is divided by head and tailfolding into three main derived from the splanchnopleuric coelomic epithelium.
compartments. The foregut extends from the buccopharyngeal mem Throughout the gut, blood vessels, lymphatics and lymph nodes
brane to its continuation into the central midgut region via the cranial develop from local populations of angiogenic mesenchyme. The nerves,
intestinal portal. The midgut extends between the intestinal portals and, which are distributed within the enteric and autonomic systems, are
in the early embryo, is in wide communication with the yolk sac. The derived from the neural crest. There is a craniocaudal developmental
hindgut extends from the caudal intestinal portal to the cloacal mem gradient along the gut, in that the stomach and small intestine develop
brane. The cranial end of the foregut, the embryonic pharynx, is in advance of the colon.
intimately associated with head and neck development (Ch. 36). The Figure 60.1 shows the fundamental relationship of the intraembry
portion of foregut that passes dorsal to the pericardial cavity gives rise onic coelom to the developing gut. Figure 60.2 shows the gut in a stage
to the respiratory diverticulum and oesophagus within the thorax (Chs 12 embryo in relation to the other developing viscera, especially the
36 and 52). Caudal to the developing diaphragm, the enteric gut is heart and liver. Figure 60.3 shows the overall development of the gut
conventionally subdivided into three embryological portions: fore, from stages 13 to 17. These diagrams should be compared.
mid and hindgut. There are no corresponding fundamental morpho All regions of the gut develop from epithelial–mesenchymal inter
logical and cytological distinctions between the three parts (Fig. 60.1), actions that are dependent on the sequential expression of a range of


and so the foregut produces a portion of the duodenum, as does the basic and specific genes; on the regulation of the developmental clock,
midgut, and the midgut similarly produces large intestine, as does the seen in all areas of development; and on endogenous regulatory mecha
hindgut. The differences between the portions of the gut develop as a nisms and local environmental influences (Lebenthal 1989). Although
result of interactions between the three embryonic tissue layers that give all these factors pertain to the whole range of developing tissues, local
rise to the gut: namely, the endodermal inner epithelium, the thick layer differences in any one of these factors along the length of the develop
of splanchnopleuric mesenchyme, and the outer layer of proliferating ing gut promote the differentiation of, for example, the gastric mucosa
splanchnopleuric coelomic epithelium. and hepatocytes; the rotation of the midgut; and the final disposition
The epithelial layer of the mucosa and connected ducts and glands of the sessile portions of the fully formed gastrointestinal tract. The
are derived from the endodermal epithelium. The lamina propria and hedgehog (Hh) ligands, Shh, Ihh and Dhh are expressed in the develop
ing gut: Shh and Ihh in the endodermal epithelium and Dhh in
endothelial cells. These ligands bind to the Patched receptors (Ptch1
and Ptch2), which activate the transcription factor Gli3. Knockout of
Shh and Ihh has been associated with oesophageal atresia, gut malrota
tion, decreased development of the muscularis propria, enteric neurone
anomalies and imperforate anus (Kolterud et al 2009). The gut is func
tional prior to birth and able to interact with the extrauterine environ
Pharynx ment in preterm infants.
OESOPHAGUS
Pericardial cavity
Foregut The oesophagus can be distinguished from the stomach at stage 13
(embryo length 5 mm). It elongates during successive stages and its
absolute length increases more rapidly than the embryo as a whole.
Pericardioperitoneal canals Cranially, it is invested by splanchnopleuric mesenchyme posterior to


the developing trachea and, more caudally, between the developing
Septum transversum lungs and pericardioperitoneal canals posterior to the pericardium.
Caudal to the pericardium, the terminal, pregastric segment of the
Body wall, oesophagus has a short, thick, dorsal mesooesophagus (from splanch
somatopleuric mesenchyme Midgut nopleuric mesenchyme), while ventrally, it is enclosed in the cranial
and coelomic epithelium
stratum of the septum transversum mesenchyme. Each of the above is
continuous caudally with its respective primitive dorsal and ventral
mesogastria. Thus, the oesophagus has only limited areas related to a
Epithelium of midgut,
splanchnopleuric mesenchyme primary coelomic epithelium. However, it is important to note the
and coelomic epithelium subsequent development of the paraoesophageal right and left pneu
Peritoneal cavity matoenteric recesses (see Fig. 60.7), the relation of the ventral aspect of
the middle third of the oesophagus to the oblique sinus of the pericar
dium, and the relation of its lateral walls in the lower thorax to the
mediastinal pleura. All the foregoing are secondary extensions from the
primary coelom.
Hindgut
The oesophageal mucosa consists of two layers of cells by stage 15
Allantois (week 5), but the proliferation of the mucosa does not occlude the
lumen at any time. The mucosa becomes ciliated at 10 weeks, and strati
Fig. 60.1 Major epithelial populations within the early embryo. The fied squamous epithelium is present at the end of the fifth month;
early gut tube is close to the notochord and neural tube dorsally. The occasionally, patches of ciliated epithelium may be present at birth.
splanchnopleuric layer of the intraembryonic coelomic epithelium is in Circular muscle can be seen at stage 15 but longitudinal muscle has not
contact with the foregut ventrally and laterally, with the midgut laterally, been identified until stage 21. Neuroblasts can be demonstrated in the


1048 and the hindgut ventrally and laterally. early stages; the myenteric plexuses have cholinesterase activity by


Postpharyngeal foregut
1049
06
RETPAHC
A Amniotic cavity B Atrioventricular canal
Median thyroid rudiment Left atrium
Pharynx
Otocyst
Bulbus Amniotic
Pharynx cordis cavity
(right
Median ventricle) Lung bud
thyroid
Left horn
rudiment Left
Lung bud ventricle of sinus
venosus
Optic
Foregut
rudiment Septum Foregut
Liver transversum
Stomodeum, diverticulum Liver
oronasal cavity Yolk duct diverticulum
Hepatic
Pericardial cavity trabeculae Gallbladder
Left vitelline vein
rudiment
Yolk stalk Gallbladder
rudiment Left umbilical artery Upper limb
Postanal gut Upper limb bud
bud Peritoneal cavity
Cloacal membrane Midgut
Midgut Cloacal membrane
Notochord
Cloaca
Hindgut Allantois Hindgut Allantois
Fig. 60.2 A, The digestive tube of a human embryo at stage 12, with 29 paired somites, a crown to rump length of 3.4 mm and an estimated age of
27 days. (Pharyngeal development is followed further in Figure 36.18.) B, Reconstruction of a human embryo at the end of the fourth week. The
alimentary canal and its outgrowths are shown in median section. The brain is shown in outline but the spinal cord has been omitted. The heart is shown
in perspective, and the left horn of the sinus venosus is cut just medial to the entrance of the common cardinal vein (see Fig. 52.8A–B). The somites are
indicated in outline.
9.5 weeks and ganglion cells are differentiated by 13 weeks. It has been ous with the dorsal mesentery (mesenteron) of almost all of the remain
suggested that the oesophagus is capable of peristalsis in the first tri der of the intestine, except its caudal short segment.
mester. Periodic fetal swallowing can be seen on ultrasound from In human embryos of 10 mm (stages 15–16), the characteristic
16 weeks. The volume of amniotic fluid ingested increases during the gastric curvatures are already recognizable. Growth is more active along


third trimester to more than 500 ml/day. Oesophageal atresia is one of the dorsal border of the viscus; its convexity markedly increases and the
the more common obstructive conditions of the alimentary tract; it may rudimentary fundus appears. Because of more rapid growth along
be indicated by polyhydramnios. There is evidence of maturation of the the dorsal border, the pyloric end of the stomach turns ventrally and
lower oesophageal sphincter at 32 weeks, when, with the prevention of the concave lesser curvature becomes apparent (see Figs 60.3, 60.6). The
free gastrooesophageal reflex, stomach size increases (Hitchcock et al stomach is now displaced to the left of the median plane and, appar
1992). ently, becomes physically rotated, which means that its original right
surface becomes dorsal and its left surface becomes ventral. Accordingly,
Oesophagus at birth the right vagus is distributed mainly to the dorsal, and the left vagus
mainly to the ventral, surfaces of the stomach. The dorsal mesogastrium
increases in depth and becomes folded on itself. The ventral mesogas
At birth, the oesophagus extends 8–10 cm from the cricoid cartilage to
trium becomes more coronal than sagittal. The pancreaticoenteric
the gastric cardiac orifice. It starts and ends one to two vertebrae, respec
recess (see Fig. 60.7B(ii)), until this point usually described as a simple
tively, higher than in the adult, extending from between the fourth to
depression on the right side of the dorsal mesogastrium, becomes
the sixth cervical vertebra to the level of the ninth thoracic vertebra (see
dorsal to the stomach and excavates downwards and to the left between
Fig. 14.7). Its average diameter is 5 mm and it possesses the constric
the folded layers. It may now be termed the inferior recess of the bursa
tions seen in the adult. The narrowest constriction is at its junction with
omentalis. Put simply, the stomach has undergone two ‘rotations’. The
the pharynx, where the inferior pharyngeal constrictor muscle functions
first is 90° clockwise, viewed from the cranial end; the second is 90°


to constrict the lumen; this region may be easily traumatized with
clockwise, about an anteroposterior axis. The displacement, morpho
instruments or catheters. In the neonate, the mucosa may contain scat
logical changes and apparent ‘rotation’ of the stomach have been attrib
tered areas of ciliated columnar epithelium but these disappear soon
uted variously to its own and surrounding differential growth changes;
after birth. Peristalsis along the oesophagus and at the lower oesopha
extension of the pancreaticoenteric recess with changes in its mesen
geal sphincter is immature at birth and results in frequent regurgitation
chymal walls; and pressure, particularly that exerted by the rapidly
of food in the newborn period. The pressure at the lower oesophageal
growing liver.
sphincter approaches that of an adult at 3–6 weeks of age.
Mucosa
STOMACH
Mucosal and submucosal development can be seen in the eighth to
At the end of the fourth and beginning of the fifth weeks, the stomach ninth weeks. No villi form in the stomach, unlike in other regions of
can be recognized as a fusiform dilation cranial to the wide opening of the gut; instead, glandular pits can be seen in the body and fundus.
the midgut into the yolk sac (see Figs 60.2 and 60.3). By the fifth week, These develop in the pylorus and cardia by weeks 10 and 11, when
this opening has narrowed into a tubular vitelline intestinal duct, which parietal cells can be demonstrated. Although acid secretion has not
soon loses its connection with the digestive tube. At this time, the been demonstrated in the fetal stomach before 32 weeks’ gestation,
stomach is median in position and separated cranially from the peri preterm infants, from 26 weeks’ gestation onwards, are able to secrete
cardium by the septum transversum (see Fig. 60.5A), which extends acid soon after birth. Intrinsic factor has been detected after 11 weeks.
caudally on to the cranial side of the vitelline intestinal duct and ven This increases from the fourteenth to the twentyfifth week, at which


trally to the somatopleure. Dorsally, the stomach is related to the aorta time the pylorus, which contains more parietal cells than it does in the
and, reflecting the presence of the pleuroperitoneal canals on each side, adult, also contains a relatively larger quantity of intrinsic factor. The
is connected to the body wall by a short dorsal mesentery, the dorsal significance of the early production of intrinsic factor and the late pro
mesogastrium (see Figs 60.5B and 60.6). The latter is directly continu duction of acid by the parietal cells is not known. Chief cells can be


DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE
1050
8
noiTCEs
Site of palatine tonsil Thymus
A B
Pharyngeal pouches
Tubotympanic recess
Inferior parathyroid
Adenohypophysial pouch
Ultimobranchial body
Lateral thyroid
Pharynx Internal carotid artery Superior parathyroid
Thyroid Lung bud
Pulmonary artery
Groove for sinus venosus Stomach Aortic sac
Oesophagus
Septum transversum Dorsal pancreas Trachea Lung
Umbilical vesicle stalk Gallbladder Pulmonary vein Stomach
Allantois Cut ends of hepatic trabeculae
Junction of yolk sac Gallbladder Dorsal pancreas
and intestine Postanal gut Bile duct
Urachus
Mesonephric duct
Umbilical vesicle stalk
Urorectal cleavage line Cloacal membrane Junction of umbilical vesicle
and intestine
Metanephros and ureter Approximate junction of colon and ileum
Mesonephric duct
C Adenohypophysis Thyroid
D
E
Aortic sac
Oesophagus
Trachea Oesophagus
Left primary bronchus Trachea Left primary bronchus
and branches
Umbilical vesicle stalk Hepatic ducts
Trachea
Primary intestinal loop Gallbladder Stomach Oesophagus
Ventral pancreas
Urogenital Urachus Dorsal pancreas
sinus
Stomach
Caecum
Gallbladder
Metanephros Mesonephric duct Hepatic ducts
Bile duct
Caecum Dorsal pancreas
Ventral pancreas Fundus of stomach
Pyloric atrium
Bladder
Hepatic ducts
Body of stomach
Gallbladder
Mesentery Primary intestinal loop
Dorsal pancreas
Mesonephric duct
Ureter Bile duct Ventral pancreas
Metanephros
Renal pelvis
(cranial and caudal poles)
Vermiform appendix
Urachus
Colon
Bladder
Metanephric kidney
0.2 mm
Collecting tubules
Ureter Mesonephric duct


Fig. 60.3 The shape of the endodermal epithelium of the gut at succeeding stages. The scale is constant, illustrating the enormous growth of the
gut over a 13-day period. A, Stage 13. B, Stage 14. C, Stage 15. D, Stage 16. E, Stage 17. Note the separation of the respiratory diverticulum; the
elongation of the foregut and expansion of the stomach; the formation of the hepatic and pancreatic diverticula; the lengthening of the midgut loop,
which protrudes into the umbilical cord; and the separation of the cloaca into enteric and allantoic portions. (Modified from O’Rahilly and Müller.
Developmental Stages in Human Embryos 1987 Carnegie Institution of Washington. Pub 637.)


Postpharyngeal foregut
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identified after weeks 12–13, although they cannot be demonstrated to atresia), or with anomalies of the bile duct. In 40–60% of cases, the
contain pepsinogen until term. Mucous neck cells actively produce atresia is complete and pancreatic tissue fills the lumen. The condition
mucus from week 16. Gastrinproducing cells have been demonstrated can be diagnosed on ultrasound examination, which reveals a typical
in the antrum between 19 and 20 weeks, and gastrin levels have been double bubble appearance, caused by fluid enlarging the stomach and
measured in cord blood and in the plasma at term. Cord serum con the proximal duodenum. Polyhydramnios is invariably present and
tains gastrin levels 2–3 times higher than those in maternal serum. often is the indication for the scan. Duodenal atresia commonly occurs
with other developmental defects, e.g. cardiac and skeletal anomalies,
Muscularis and in Down’s syndrome.
The stomach muscularis externa develops its circular layer at 8–9 weeks,
DORSAL AND VENTRAL MESENTERIES
when neural plexuses are developing in the body and fundus. The
longitudinal muscle develops slightly later. Few studies note a time of OF THE FOREGUT
appearance of the oblique layer. The pyloric musculature is thicker than
the rest of the stomach; in general, the thickness of the total muscula The epithelium of the stomach and duodenum does not rotate relative
ture of the stomach at term is reduced, compared to the adult. to its investing mesenchyme. The rotation includes the coelomic epi
thelial walls of the pericardioperitoneal canals, which are on each side
Serosa of the stomach and duodenum and form its serosa, and the elongating
dorsal mesogastrium or the much shorter dorsal mesoduodenum. A
ventral mesogastrium can be seen when the distance between the
The serosa of the stomach is derived from the splanchnopleuric coe
stomach and liver increases. Whereas the dorsal mesogastrium takes
lomic epithelium. No part of this serosa undergoes absorption. The


origin from the posterior body wall in the midline, its connection to
original left side of the gastric serosa faces the greater sac; the right side
the greater curvature of the stomach, which lengthens as the stomach
faces the lesser sac.
grows, becomes directed to the left as the stomach undergoes its first
Stomach at birth rotation. With the second rotation, a portion of the dorsal mesogas
trium now faces caudally (see Fig. 60.6). The ventral mesogastrium
remains as a double layer of coelomic epithelium, which encloses mes
The stomach exhibits fetal characteristics until just after birth, when the
enchyme and forms the lesser omentum (see Fig. 60.7).
initiation of pulmonary ventilation, the reflexes of coughing and swal
Movement of the stomach is associated with an extensive lengthen
lowing, and crying cause the ingestion of large amounts of air and
ing of the dorsal mesogastrium, which becomes the greater omentum;
liquid. Once postnatal swallowing has started, the stomach distends to
this now, from its posterior origin, droops caudally over the small
four or five times its contracted state, and shifts its position in relation
intestine, then folds back anteriorly and ascends to the greater curvature
to the state of expansion and contraction of the other abdominal
of the stomach. The greater omentum is, therefore, composed of a fold
viscera, and to the position of the body. In the neonate, the anterior
containing, technically, four layers of peritoneum. The dorsal mesoduo
surface of the stomach is generally covered by the left lobe of the liver,
denum, or suspensory ligament of the duodenum, is a much thicker
which extends nearly as far as the spleen (see Fig. 14.6B). Only a small
structure, and it fixes the position of the duodenum when the rest of
portion of the greater curvature of the stomach is visible anteriorly. The
the midgut and its dorsal mesentery elongate and pass into the umbili
capacity of the stomach is 30–35 ml in the fullterm neonate, rising to
cal cord.
75 ml in the second week and 100 ml by the fourth week (adult capac


ity is, on average, 1000 ml). The mucosa and submucosa are relatively
thicker than in the adult; however, the muscularis is only moderately
SPECIAL GLANDS OF THE
developed and peristalsis is not coordinated. At birth, gastric acid secre
POSTPHARYNGEAL FOREGUT
tion is low, which means that gastric pH is high for the first 12 postnatal
hours. It falls rapidly with the onset of gastric acid secretion, usually
Pancreas
after the first feed. Acid secretion usually remains low for the first
10 days postnatally. Gastric emptying and transit times are delayed in
the neonate. The pancreas develops from two evaginations of the foregut that fuse
to form a single organ. A dorsal pancreatic bud can be seen in stage 13
embryos as a thickening of the endodermal tube that proliferates into
DUODENUM the dorsal mesogastrium (see Fig. 60.3; Fig. 60.4). A ventral pancreatic
bud evaginates in close proximity to the liver primordium but cannot
The duodenum develops from the caudal part of the foregut and the be clearly identified until stage 14, when it appears as an evagination
cranial part of the midgut. A ventral mesoduodenum, which is continu of the bile duct itself. At stage 16 (5 weeks), differential growth of the
ous cranially with the ventral mesogastrium, is attached only to the wall of the duodenum results in movement of the ventral pancreatic
foregut portion. Posteriorly, the duodenum has a thick dorsal mesoduo bud and the bile duct to the right side and, ultimately, to a dorsal posi
denum, which is continuous with the dorsal mesogastrium cranially tion. It is not clear whether there is a corresponding shift of mesen
and the dorsal mesentery of the midgut caudally. Anteriorly, the extreme chyme during this rotation. However, the ventral pancreatic bud and
caudal edge of the ventral mesentery of the foregut extends on to the the bile duct rotate from a position within the ventral mesogastrium


short initial segment of the duodenum. The liver arises as a diverticu (ventral mesoduodenum) to one in the dorsal mesogastrium (dorsal
lum from the ventral surface of the duodenum at the foregut–midgut mesoduodenum), which is destined to become fixed on to the posterior
junction, i.e. where the midgut is continuous with the yolk sac wall (the abdominal wall. By stage 17, the ventral and dorsal pancreatic buds
cranial intestinal portal). The ventral pancreatic bud also arises from have fused, although the origin of the ventral bud from the bile duct is
this diverticulum. The dorsal pancreatic bud evaginates posteriorly into still obvious. Threedimensional reconstruction of the ventral and
the dorsal mesoduodenum slightly more cranially than the hepatic dorsal pancreatic buds has confirmed that the dorsal pancreatic bud
diverticulum. The rotation, differential growth, and cavitations related forms the anterior part of the head, the body and the tail of the pan
to the developing stomach and omenta cause corresponding move creas, and the ventral pancreatic bud forms the posterior part of the
ments in the duodenum, which forms a loop directed to the right, with head and the posterior part of the uncinate process. The ventral pan
its original right side now adjacent to the posterior abdominal wall (see creatic bud does not form all of the uncinate process (Collins 2002a).
Fig. 60.6). This shift is compounded by the migration of the bile duct The developing pancreatic ducts usually fuse in such a way that most
and ventral pancreatic duct around the duodenal wall. Their origin of the dorsal duct drains into the proximal part of the ventral duct (see
shifts until it reaches the medial wall of the second part of the fully Figs 60.3–60.4). The proximal portion of the dorsal duct usually per
formed duodenum; the bile duct passes posteriorly to the duodenum sists as an accessory duct. The fusion of the ducts takes place late in
and travels in the free edge of the ventral duodenum and ventral meso development or in the postnatal period; 85% of infants have patent
gastrium. Local adherence and subsequent absorption of part of the accessory ducts, as compared to 40% of adults. Fusion may not occur


duodenal serosa and the parietal peritoneum result in almost the whole in 10% of individuals, in which case separate drainage into the duode
of the duodenum, other than a short initial segment, becoming retro num is maintained: socalled pancreatic divisum (pancreas divisum).
peritoneal (sessile). Failure of the ventral pancreatic diverticulum to migrate will result in
Duodenal atresia is a developmental defect found in 1 in 5000 live an anular pancreas, which may constrict the duodenum locally.
births (Whittle 1999). It may be associated with an anular pancreas, The ventral pancreas does not always extend anterior to the superior
which may compress the duodenum externally (20% of duodenal mesenteric vein but remains related to its right lateral surface. Initially,


DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE
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A ductules, which terminate as blindending acini or as tubular, acinar
elements.
Oesophagus
The ductal branching pattern and acinar structure of the pancreas
are determined by the pancreatic mesenchyme. This mesenchyme gives
rise to connective tissue between the ducts, which, in the fetus, appears
to be important in stimulating pancreatic proliferation and maintaining
the relative proportions of acinar, α and β cells during development. It
also provides cell lines for smooth muscle within the pancreas. Ang
iogenic mesenchyme invades the developing gland to produce blood
and lymphatic vessels.
Stomach
The process of islet differentiation is divided into two phases (Collins
2002a). Phase I, characterized by proliferation of polyhormonal cells,
Hepatic ducts
occurs from weeks 9–15. Phase II, characterized by differentiation of
monohormonal cells, is seen from week 16 onwards. The β cells, pro
ducing insulin and amylin, differentiate first, followed by α cells, which
Gallbladder Duodenum produce glucagon. The δ cells, which produce somatostatin, are seen
after 30 weeks. The dorsal bud gives rise mostly to α cells, and the
ventral bud to most of the pancreatic polypeptideproducing cells. The
Ventral pancreatic outgrowth
Dorsal pancreatic β cells develop from the duct epithelium throughout development and
outgrowth into the neonatal period. Later, in weeks 10–15, some of the primitive
ducts differentiate into acinar cells, in which zymogen granules or
acinar cell markers can be detected at 12–16 weeks.
The pancreas in the neonate has all of the normal subdivisions of
the adult. The head is proportionately large in the newborn and there
B Accessory duct (dorsal rudiment) Pyloric antrum is a smooth continuation between the body and the tail. The inferior
Stomach border of the head of the pancreas is found at the level of the second
lumbar vertebra. The body and tail pass cranially and to the left, and


Biliary duct the tail is in contact with the spleen (see Fig. 14.6).
Liver
The liver is one of the most precocious embryonic organs and is the
Cystic duct Dorsal pancreas main centre for haemopoiesis in the fetus. It develops from an endo
dermal evagination of the foregut and from septum transversum mes
enchyme, which is derived from the proliferating coelomic epithelium
in the protocardiac region. The development of the liver is intimately
related to the development of the heart. The vitelline veins, succeeded
by the umbilical veins passing to the sinus venosus, are disrupted by
Bile duct the enlarging septum transversum to form a hepatic plexus, the forerun
ner of the hepatic sinusoids. (See Collins (2002b) for a detailed account
Portal vein of hepatic development.)
Principal duct (ventral rudiment)
Early liver development
Fig. 60.4 Development of the pancreas in a human embryo. A, An early
As the head fold and early intraembryonic coelom form, the ventral
stage, 7.5 mm embryo: lateral view. B, A later stage, 14.5 mm embryo:
ventral view. parietal wall of the pericardial cavity gives rise to populations of cells
termed precardiac or cardiac mesenchyme. Hepatic endoderm is
induced to proliferate by this mesenchyme, although all portions of the
the body of the pancreas extends into the dorsal mesoduodenum and early heart tube, truncus arteriosus, atria, ventricle, both endocardium
then cranially into the dorsal mesogastrium. As the stomach rotates, and myocardium, have hepatic induction potency that is tissuespecific
this portion of the dorsal mesogastrium is directed to the left, forming but not speciesspecific. As the heart and foregut become separated by
the posterior wall of the lesser sac. The posterior layer of this portion the accumulation of the cardiac mesenchyme, the mesenchyme itself is
of dorsal mesogastrium fuses with the parietal layer of the coelom wall renamed septum transversum. It is seen as a ventral mass, caudal to the


(peritoneum), and the pancreas becomes mainly retroperitoneal (see heart, which passes dorsally on each side of the developing gut to join
Fig. 60.7C). The region of fusion of the dorsal mesogastrium does not the mesenchyme proliferating from the walls of the pericardioperito
extend so far left as to include the tail of the pancreas, which passes neal canals. The majority of the cells within the septum transversum
into the splenorenal (lienorenal) ligament. The anterior border of the are destined to become hepatic mesenchyme. For details of the molecu
pancreas later provides the main line of attachment for the posterior lar signalling of early hepatic development, see Lemaigre (2009).
leaves of the greater omentum. In the stage 11 embryo, the location of the hepatic endoderm has
been identified at the superior boundary of the rostral intestinal portal.
Cellular development of the pancreas
By stage 12, the hepatic endodermal primordium is directed ventrally
The early specification of pancreatic endoderm involves the proximity and begins to proliferate as a diverticulum. There are two parts: a caudal
of the notochord to the dorsal endoderm, which locally represses the part, which will produce the cystic duct and gallbladder; and a cranial
expression of Shh transcription factor. Endoderm caudal to the pancre part, which forms the liver biliary system (see Fig. 60.3; Fig. 60.5A).
atic region does not respond to notochordal signals. The ventral pan The cells start to express liverspecific molecular markers and glycogen
creatic endoderm does not seem to undergo the same induction. storage.
Pancreatic mesenchyme is derived from two regions. The mesenchyme Around the cranial portion of the hepatic diverticulum, the basal
that surrounds the dorsal pancreatic bud proliferates from the splanch lamina is progressively disrupted and individual epithelial cells migrate
nopleuric coelomic epithelium of the medial walls of the pericardio into the surrounding septum transversum mesenchyme. The previously
peritoneal canals, whereas the ventral pancreatic bud is invested by smooth contour of the diverticulum merges into columnar extensions


septum transversum mesenchyme and by mesenchyme derived from of endoderm, the epithelial trabeculae, which stimulate the hepatic
the lower ventral walls of the pericardioperitoneal canals. mesenchymal cells to form blood islands and endothelium. The
The primitive endodermal ductal epithelium provides the stem cell advance of the endodermal epithelial cells promotes the conversion of
population for all the secretory cells of the pancreas. Initially, these progressively more hepatic mesenchyme into endothelium and blood
endocrine cells are located in the duct walls or in buds developing from cells, and only a little remains to form the scanty liver capsule and
them; later, they accumulate in pancreatic islets. The remaining primi interlobular connective tissue. This invasion by the hepatic epithelium
tive duct cells will differentiate into definitive ductal cells. In the fetus, is completed in stage 13, when it approaches the caudal surface of the
they develop microvilli and cilia but lack the lateral interdigitations pericardial cavity, and is separated from it only by a thin lamina of
seen in the adult. Branches of the main duct become interlobular mesenchyme that will give rise to part of the diaphragm.


Postpharyngeal foregut
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A Cranial B
Foregut
Pericardial cavity
Oesophagus Lung
Lungs
Dorsal mesogastrium
Septum transversum Pericardio- Ventral mesogastrium
peritoneal canals
Dorsal aorta
Liver developing within
Hepatic trabeculae
septum transversum
Spleen
Putative common bile duct
Gallbladder
Biliary duct system
Dorsal
Fig. 60.5 Early development of the liver and the supra-umbilical peritoneal
cavities. A, The hepatic endodermal primordium proliferates ventrally into
Ventral
the septum transversum mesenchyme. The endodermal cells forming the
hepatic trabeculae will become hepatocytes; the septum transversum
mesenchymal cells will become the endothelium of the liver sinusoids
and early blood cells. The developing lung buds can be seen expanding
C Oesophagus Stomach
into the pericardioperitoneal cavities. B, The septum transversum
Spleen mesenchyme and the stomach become enclosed by the right and left
pericardioperitoneal canals (shown on transverse section). The apposition
of the medial pericardioperitoneal walls forms the dorsal and ventral
Developing liver mesogastria. The proximity of the lung buds to the developing stomach
Ventral
can be seen. The pleural and supra-umbilical peritoneal cavities are
pancreatic
bud transiently, and bilaterally, symmetrical above the umbilicus. C, The lower
border of the ventral mesogastrium denotes the connection between the
supra-umbilical peritoneal cavities: pleuroperitoneal canals, which can be
Dorsal
pancreatic identified by the position of the ventral pancreatic bud and common bile
bud duct. The white arrows in B and C indicate the direction of movement of
the dorsal and ventral mesogastria.
During this early phase of development, the liver is far more highly diverticulum gives rise to the liver hepatocytes, the intrahepatic large


vascularized than the rest of the gut. The hepatic capillary plexus is bile ducts (right and left hepatic ducts, segmental ducts, area ducts and
connected bilaterally with the right and left vitelline veins. Dorsolater their first branches) and the small bile ducts (septal bile ducts, inter
ally, they empty by multiple channels into enlarged hepatocardiac chan lobular ducts and bile ductules). The portal and hepatic veins arise
nels, which lead to the right and left horns of the sinus venosus (see together from the vitelline veins. Early in development, the accumula
Fig. 60.9); usually, the channel on the right side is most developed. tion of mesenchyme around these veins is similar, whereas later mes
Both left and right channels bulge into the pericardioperitoneal canals, enchyme increases around the portal veins. This is a prerequisite for
forming sites for the exchange of fluid from the coelom into the vascular bile duct development. Primitive hepatocytes surround the portal vein
channels. The growth of the hepatic tissue in these regions is sometimes branches and associated mesenchyme, and form a sleeve of cells termed
referred to as the left and right horns of the liver. the ductal plate. Individual cells of the ductal plate are termed cholan
The liver remains proportionately large during its development and giocytes. Local hepatoblasts that are adjacent to the cholangiocytes
constitutes a sizeable organ dorsal to the heart at stage 14, then more arrange themselves to delineate a bile duct lumen and then also switch
caudally placed by stage 16. By this stage, hepatic ducts can be seen to a cholangiocyte lineage (Lemaigre 2009). As the bile ducts develop,
separating the hepatic epithelium from the extrahepatic biliary system, angiogenic mesenchymal cells form blood vessels that connect to the
but, even at stage 17, the ducts do not penetrate far into the liver. hepatic artery from 10 weeks. Thus, the portal triads are patterned by
the portal vein radicles, which initially induce bile duct formation and
Maturation of the liver
then artery formation. The development of the biliary system extends


At 3 months’ gestation, the liver almost fills the abdominal cavity and from the hilum to the periphery. Anomalies of the biliary tree are associ
its left lobe is nearly as large as its right. When the haemopoietic activity ated with abnormalities of the branching pattern of the portal vein. The
of the liver is assumed by the spleen and bone marrow, the left lobe developing bile ducts remain patent throughout development; the solid
undergoes some degeneration and becomes smaller than the right. The stage of ductal development previously promulgated has been refuted.
liver remains relatively larger than in the adult throughout the remain Atresia of the extrahepatic bile ducts has been noted, often in associa
der of gestation. In the neonate, it constitutes 4% of the body weight, tion with extrahepatic atresia. The cause of this condition is not clear;
compared to 2.5–3.5% in adults. It is in contact with the greater part inflammatory process may be involved, although some cases have fea
of the diaphragm and extends below the costal margin anteriorly, and, tures of ductal plate malformation (Howard 2002).
in some cases, to within 1 cm of the iliac crest posteriorly. The left lobe
Development of extrahepatic biliary ducts
covers much of the anterior surface of the stomach and constitutes
nearly onethird of the liver (see Fig. 14.6). Although its haemopoietic The caudal part of the hepatic endodermal diverticulum forms the
functions cease before birth, its enzymatic and synthetic functions are extrahepatic biliary system, the common hepatic duct, gallbladder,
not completely mature at birth. Hepatocytes remain a heterogeneous cystic duct and common bile duct.
population with different gene expressions and metabolic functions The bile duct, which originated from the ventral wall of the foregut
within different hepatic lobule locations. This metabolic zonation (now duodenum), migrates with the ventral pancreatic bud, first to the
becomes fully established after birth (Lemaigre 2009). right and then dorsomedially into the dorsal mesoduodenum. The right
and left hepatic ducts arise from the cranial end of the common hepatic
Development of intrahepatic biliary ducts
duct from 12 weeks’ gestation.


The development of the intrahepatic biliary ducts follows the branching Atresia of the extrahepatic bile ducts in neonates occurs alone or in
pattern of the portal vein radicles (Collins 2002b). The cranial hepatic conjunction with a range of other anomalies, including situs inversus,


DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE
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malrotation, polysplenia and cardiac defects. In such cases, the intra sure; these hernias usually resolve without treatment. Exomphalos is a
hepatic bile ducts have a mature tubular shape but also show features ventral wall defect with midline herniation of the intraabdominal
of ductal plate malformation. contents into the base of the umbilical cord. Herniated viscera are
In the neonate, the gallbladder has a smaller peritoneal surface than covered by the peritoneum internally and amnion externally. The
in the adult, and its fundus often does not extend to the liver margin. omphalocele so formed ranges in size from a large umbilical hernia to
It is generally embedded in the liver and, in some cases, may be covered a very large mass containing most of the visceral organs. Even after the
by bands of liver. After the second year, the gallbladder assumes the exomphalos has been repaired, these babies will still have a deficient
relative size it has in the adult. anterior abdominal wall.
Gastroschisis is a paraumbilical defect of the anterior abdominal
wall associated with evisceration of the abdominal organs. The organs
MIDGUT are not enclosed in membranes; thus, gastroschisis can be detected by
prenatal ultrasonography and differentiated from exomphalos (see Fig.
14.5B). Gastroschisis is thought to result from periumbilical ischaemia,
The midgut forms the third and fourth parts of the duodenum, jejunum,
caused by vascular compromise of either the umbilical vein or arteries.
ileum and twothirds of the way along the transverse colon; its develop
The incidence of this condition appears to be increasing, especially in
ment produces most of the small, and a portion of the large, intestine.
babies born to young women less than 20 years old (Whittle 1999,
In embryos of stages 10 and 11, it extends from the cranial to the caudal
Ionescu et al 2014).
intestinal portals and communicates directly with the yolk sac over its


Congenital volvulus arises if the midgut loop does not rotate appro
entire length. Although it has a dorsal wall, the lateral walls have not
priately. A number of types of this condition are identified. Leftsided
yet formed at these stages. By stage 12, the connection with the yolk
colon occurs if the midgut loop has not rotated at all; mixed rotation
sac has narrowed, such that the midgut has ventral walls cranially and
results in the caecum lying inferior to the pylorus; and failure of appro
caudally. This connection is reduced to a yolk stalk containing the vitel
priate attachment of the peritoneum may result in the small intestine
lointestinal duct during stage 13, at which time the yolk sac appears as
being attached at only two points on the posterior abdominal wall. All
a sphere in front of the embryo. Posterior to the midgut, the splanch
of these arrangements lead to a risk of volvulus, which may result in
nopleuric coelomic epithelia converge, forming the dorsal mesentery.
necrosis of the gut.
Ventrolaterally, the intraembryonic coelom is in wide communication
The position and configuration of the duodenal loop are of particu
with the extraembryonic coelom. At stage 14, the midgut has increased
lar importance in children. The normal duodenal loop has a Ushaped
in length more than the axial length of the embryonic body and, with
configuration. The suspensory ligament of the duodenum (ligament of
elongation of the dorsal mesentery, it bulges ventrally, deviating from
Treitz) is usually found to the left of the body of the first or second
the median plane. For all these stages, see Figure 60.3.
lumbar vertebral body after normal gut rotation; any other position of
this ligament may indicate some degree of gut malrotation. On barium
PRIMARY INTESTINAL (OR MIDGUT) LOOP studies, the duodenojejunal flexure should, thus, lie to the left of the
upper lumbar spine at the level of the pylorus.
If the caecum has remained in the right upper quadrant, it may


The midgut loop can first be seen at stage 15, when a bulge – the caecal
become fixed in that position by peritoneal attachments passing to the
bud – can be discerned on the lower limb of the loop, caudal to the
right, the socalled Ladd’s bands. These may compress the underlying
yolk stalk (which arises from the apex or summit of the loop). Later,
duodenum and give rise to duodenal stenosis. The high positioning of
the original proximal limb of the loop moves to the right and the distal
the caecum close to the duodenal jejunal flexure – in some cases, in the
limb to the left (see Fig. 60.3C). The longest portion of the dorsal
midline – is associated with later development of volvulus.
mesentery is at the level of the yolk stalk; there is less relative lengthen
The identification of intestinal malrotation can be made by Xray
ing near the caudal end of the duodenum or the cranial half of the
investigation. However, ultrasonography has the advantage of showing
colon. The midgut extends into the umbilical coelom, having already
the position of the superior mesenteric vein and artery. The vein should
rotated through an angle of 90° (anticlockwise, viewed from the ventral
lie to the right of the artery. Most cases of volvulus will show inversion
aspect). This relative position is approximately maintained so long as
of this normal relationship but malrotation can occur with apparently
the protrusion persists, during which time the proximal limb that forms
normally related vessels, particularly in malrotation with bowel obstruc
the small intestine elongates greatly. It becomes coiled, and its adjacent
tion due to Ladd’s bands and not volvulus.
mesentery adopts a pleated appearance. The origin of the root of the
mesentery is initially both median and vertical, while, at its intestinal
attachment, it is elongated like a ruffle and folded along a horizontal UMBILICAL CORD
zone. The mesenteric sheet and its contained vessels have spiralled
through 90°. The distal, colic, part of the loop elongates less rapidly
During the period when the midgut loop protrudes into the umbilical


and has no tendency to become coiled. By the time the fetus has
coelom, the edges of the ventral body wall are becoming relatively
attained a length of 40 mm (10 weeks), the peritoneal cavity has
closer, forming a more discrete root for the umbilical cord. Somatic
enlarged and the relative size of the liver and mesonephros is much
mesenchyme, which will form the ventral body wall musculature,
less. The reentry of the gut occurs rapidly and in a particular sequence,
migrates into the somatopleuric mesenchyme and passes ventrally
during which it continues the process of rotation. The proximal loop
towards the midline. The umbilical cord forms all of the ventral body
returns first, with the jejunum mainly on the left and the ileum mainly
wall between the pericardial bulge and the developing external genita
on the right of the subhepatic abdominal cavity. As they reenter the
lia. It encloses a portion of the extraembryonic coelom, the umbilical
abdominal cavity, the coils of jejunum and ileum slide inwards over the
coelom, into which midgut loop protrudes. When the midgut loop is
right aspect of the descending mesocolon, and so displace the descend
abruptly returned to the abdominal cavity, the more recognizable
ing colon to the left. The transverse colon passes superiorly to the origin
umbilical cord forms. The vitellointestinal duct and vessels involute.
of the root of the mesentery (Fig. 60.6). The caecum is the last to
The cranial end of the allantois becomes thinned and its lumen partially
reenter and, at first, lies on coils of ileum on the right. Later develop
obliterated, and it forms the urachus. The mesenchymal core of the
ment of the colon leads to its elongation and to the establishment of
umbilical cord is derived by coalescence from somatopleuric amniotic
the hepatic and splenic flexures. A timetable for intestinal rotation in
mesenchyme, splanchnopleuric vitellointestinal (yolk sac) mesen
staged human embryos is given by Kim et al (2003).


chyme and splanchnopleuric allantoic (connecting stalk) mesenchyme.
These various layers become fused and are gradually transformed into
Anomalies of midgut rotation the viscid, mucoid, connective tissue (Wharton’s jelly) that characterizes
the more mature cord. The changes in the circulatory system result in
If the midgut loop fails to return to the abdominal cavity at the appro a large, cranially orientated, left umbilical vein (the right umbilical vein
priate time, a range of ventral defects can result. Failure of obliteration regresses), and two spirally disposed umbilical arteries (see Fig. 52.19).
of the vitellointestinal duct connecting the midgut to the yolk sac results
in Meckel’s diverticulum. This may present as a short segment of vitel
MATURATION OF THE SMALL INTESTINE
line duct attached to the original ventral side of the ileum; it may
remain attached to the umbilicus as a fistula; or it may remain as a liga
Mucosa
mentous attachment to the umbilicus.
An umbilical hernia occurs when loops of gut protrude into a
widened umbilical cord at term. The degree of protuberance may The exact timing of the cellular morphogenesis of the gut is difficult
increase when the infant cries, which raises the intraabdominal pres to establish, especially as it undergoes a proximodistal gradient in


midgut
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Gut tube Oesophagus Stomach
A Ventral mesogastrium Dorsal mesogastrium B Spleen
Dorsal Septum transversum
aorta
Septum transversum
Biliary duct system
Umbilical vein Dorsal
mesentery
Yolk sac
Dorsal
pancreatic
bud
Umbilical Ventral
coelom pancreatic
bud
Allantois
Rotation
Umbilical artery Midgut loop entering beginning
umbilical coelom
Caecum
Liver Lesser Gastrosplenic
C omentum ligament D
Falciform ligament
Splenorenal
ligament
Gallbladder
Gallbladder
Caecum Early epiploic foramen
Expanding
greater
omentum
Ventral
pancreatic
Colon
bud
Jejunum
and ileum
Superior mesenteric artery
(axis of midgut rotation)
Fig. 60.6 The major developmental sequences of the subdiaphragmatic embryonic and fetal guts, together with their associated major glands,
peritoneum and mesenteries: left anterolateral aspect. A–F, The development sequence spans 1.5 months to the perinatal period. A–B, The top white
arrows show the relative movements of the dorsal and ventral mesogastria that result in the longitudinal rotation of the stomach and limited entry to the
lesser sac (see also Fig. 60.5). C–D, The lower white arrows associated with the midgut indicate the relative movements and rotation of the midgut loop
within the umbilical coelom, and as it returns to the abdominal cavity.
Continued
maturation. Developmental differences between parts of the small ner’s glands are present in the duodenum from 15 weeks and the mus
intestine or colon have not yet been correlated with age. The endoder cularis mucosa can be seen in the small intestine from 18 weeks.
mal cells of the small intestine proliferate and form a layer some three Whereas mitotic figures are initially seen throughout the endoder
to four cells thick, with mitotic figures throughout. From 7 weeks, blunt mal layer of the small intestine prior to villus formation, by 10–12 weeks


projections of the endoderm have begun to form in the duodenum and they are limited to the intervillous regions and the developing crypts.
proximal jejunum; these are the developing villi, which increase in It is believed that an ‘adult’ turnover of cells may exist when roundedup
length until, in the duodenum, the lumen becomes difficult to discern. cells can be observed at the villus tips, in position for exfoliation. The
The concept of occlusion of the lumen and recanalization, which is absorptive enterocytes have microvilli at their apical borders before
described in many accounts of development, does not match the cyto 9 weeks. An apical tubular system appears at this time, and is com
differentiation that occurs in the gut epithelia. Thus, it is no longer posed of deep invaginations of the apical plasma membrane and
thought that there is secondary recanalization of the gut lumen. By membranebound vesicles and tubules; many lysosomal elements
9 weeks, the duodenum, jejunum and proximal ileum have villi, and (meconium corpuscles) appear in the apical cytoplasm. These latter
the remaining distal portion of ileum develops villi by 11 weeks. The features are more developed in the ileum than jejunum, are most
villi are covered by a simple epithelium. Primitive crypts, epithelial prominent at 16 weeks, and diminish by 21 weeks. There are abundant
downgrowths into the mesenchyme between the villi, appear between deposits of glycogen in the fetal epithelial cells, and it has been sug
10 and 12 weeks and similarly follow a craniocaudal progression. Brun gested that, prior to the appearance of hepatic glycogen, the intestinal


DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE
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E F
Duodenum is
retropositioned
Caecum
Layers of
greater
omentum
Arrows here indicate
gut undergoing
continued rotation Caecum
Transverse colon
G H
Duodenum Root of greater omentum
Spleen
Transverse
mesocolon
Ascending Ascending
colon now colon
retroperitoneal
Jejunoileal Transverse
mesentery mesocolon
Descending
Descending
colon now
colon
retroperitoneal
Sigmoid mesocolon
Sigmoid colon
Caecum
Pelvic mesocolon
Fig. 60.6, cont’d The major developmental sequences of the subdiaphragmatic embryonic and fetal guts, together with their associated major glands,
peritoneum and mesenteries: left anterolateral aspect. E–F, The lower white arrows associated with the midgut indicate the relative movements and
rotation of the midgut loop within the umbilical coelom, and as it returns to the abdominal cavity. G–H, The approximate disposition in the adult
abdomen of the gut (G) and the mesenteric roots, showing their lines of attachment and principal contained vessels (H).
epithelium serves as a major glycogen store. Goblet cells are present in contains vernix and cellular debris, salivary, biliary, pancreatic and
small numbers by 8 weeks, Paneth’s cells differentiate at the base of the intestinal secretions, and sloughed enterocytes. As the mixture passes
crypts in weeks 11 and 12, and enteroendocrine cells appear between along the gut, water and solutes are removed and cellular debris and
weeks 9 and 11. M cells (membrane or microfold cells) are present proteins concentrated. Meconium contains enzymes from the pancreas
from 14 weeks. and proximal intestine in higher concentrations in preterm than in
Intestinal subepithelial myofibroblasts (ISEMFs) have been described fullterm babies.
within the villus cores and adjacent to the intervillous space at the base


of the crypts from week 21. They are arranged as a syncytium between
Muscularis layer
the epithelium and the muscularis mucosae, where they contribute to
the extracellular matrix. They demonstrate αsmooth muscle actin
(SMA) expression (McLin et al 2009). It is not clear whether these cells The muscularis layer is derived from the splanchnopleuric mesenchyme,
derive from splanchnopleuric mesenchyme fibroblasts, smooth muscle as it is in other parts of the gut. Smooth muscle myoblasts are character
precursors or neural crest. They migrate from the crypts to the villous ized by expression of αSMA. Longitudinal muscle can be seen from
axis in a manner similar to enterocytes. 12 weeks. At 26–30 weeks, the gut shows contractions without regular
Meconium can be detected in the lumen of the intestine by the periodicity; from 30–33 weeks, repetitive groups of regular contractions
sixteenth week. It is derived from swallowed amniotic fluid, which have been seen in preterm neonates.


Primitive hindgut
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Serosa MATURATION OF THE LARGE INTESTINE
The small intestine possesses only a dorsal mesentery. The movement The similarity of development of the small and large intestines is further
of the root of this dorsal mesentery, and the massive lengthening of its mirrored in their cytological differentiation. Fetal gut, from 11 weeks,
enteric border in order to match the longitudinal growth of the gut tube, shows dipeptidase activity in the colon as well as in the small intestine.
reflect the spiralizing of the midgut loop in the umbilical coelom. Throughout preterm development, meconium corpuscles are seen in
the colon and in the small intestine; they are believed to be the phago
Small intestine at birth cytosed remains of neighbouring cells that have died as a result of
programmed cell death.
There is little direct evidence of colonic function in the human fetus
The radial patterning of the small intestine is completed before birth,
and neonate. However, the specific results of mammalian studies are
with differentiation of the crypt–villous axis. Specification of the space
being correlated to human studies where possible. A number of distinct
between villi, crypt depth and villous length is a dynamic process
and important differences between the function of adult and fetal colon
dependent on the establishment of the intestinal microbiota. In the
have been reported.
neonate, the small intestine forms an ovalshaped mass with its greater
diameter transversely orientated in the abdomen, rather than vertically
Mucosa
as in the adult. The mass of the small intestine inferior to the umbilicus
is compressed by the urinary bladder, which is anterior at this point.
The small intestine is 300–350 cm long at birth and its width, when The absorption of glucose and amino acids does not take place through
empty, is 1–1.5 cm. The ratio between the length of the small and the the colonic mucosa in adult life, but there is evidence of direct absorp
length of the large intestine at birth is similar to the adult ratio. The tion of these nutrients during development. At birth, the normal cycle
mucosa and submucosa are fairly well developed and villi are present of bile acids is not mature. In the adult, bile is secreted by the liver,


throughout the small intestine; however, some epithelial differentiation stored in the gallbladder and then secreted into the intestine, where it
is incomplete. The muscularis is very thin, particularly the longitudinal is absorbed by the jejunum and ileum. In the fetus and neonate, the
layer, and there is little elastic tissue in the wall. There are few or no transport of bile acids by an active process from the ileum does not
circular folds in the small intestine, and the jejunum and ileum have occur, and so bile salts pass on into the colon. In the adult, the presence
little fat in their mesentery. of bile salts in the colon stimulates the secretion of water and electrolytes,
which results in diarrhoeal syndrome; however, the fetal and neonatal
colon seems protected from this effect. The colon is not considered a
PRIMITIVE HINDGUT site of significant nutrient absorption in the adult, and yet neonates are
unable to assimilate the full lactose load of a normal breast feed from
the small intestine and a large proportion of it may be absorbed from
Just as the foregut has an extensive ventral endodermal diverticulum,
the colon. Thus, it appears that the colon fulfils a slightly different role
which contributes to a system separate from the gut, so, too, the hindgut
in the preterm and neonatal period, conserving nutrient absorption and
has a ventral diverticulum – the allantois – destined for a different
minimizing fluid loss until the neonate has adjusted to extrauterine life,
system. However, unlike the respiratory diverticulum of the foregut, the
oral feeding and the establishment of the symbiotic bacterial flora.
allantois is formed very early in development, prior even to formation
of the embryonic endoderm and tailfolding. With the reorganization
of the caudal region of the embryo at stage 10, part of the allantois is Muscularis
drawn into the body cavity. The early embryonic hindgut thus consists
of a dorsal tubular region extending from the caudal intestinal portal The muscularis is present and functioning by the eighth week, when
to the cloacal membrane, and a ventral blindending allantois extend peristaltic waves have been observed. The specific orientation of the


ing from the cloacal region into the connecting stalk. The slightly longitudinal muscle layer into taeniae coli occurs in the eleventh to
dilated cavity, lined by endoderm, that cranially receives the enteric twelfth weeks, when haustra appear. The enteric nerves are present in
hindgut proper and the root of the allantoenteric diverticulum is termed Meissner’s and Auerbach’s plexuses at 8 and 12 weeks, respectively;
the endodermal cloaca. It is closed ventrally by the cloacal membrane there is a craniocaudal migration of neurones into the gut wall. A
(endoderm opposed to proctodeal ectoderm), and it also has, tran normal distribution of ganglion cells has been noted in preterm babies
siently, a small recess of endoderm in the root of the tail, the postanal of 24 weeks, although there is a region devoid of ganglia just above the
gut. As elsewhere, the hindgut, allantois and endodermal cloaca are anal valves. Anomalous migration of neural crest cells to the gut may
encased in splanchnopleuric mesenchyme. Proliferation of the mesen give rise to Hirschsprung’s disease (see below). Puborectalis appears in
chyme and endoderm in the angle of the junction of hindgut and 20–30 mm embryos, following opening of the anal membrane.
allantois produces a urorectal septum (see Fig. 72.4B). Continued pro
liferation of the urorectal septum and elongation of the endodermal Serosa
structures thrust the endodermal epithelium towards the cloacal mem
brane, with which it fuses centrally, separating the presumptive rectum
The development of the serosa of the intestine is considered with the
and upper anal canal (dorsally) from the presumptive urinary bladder
development of the peritoneal cavity (see below).
and urogenital sinus (ventrally) (see Fig. 72.4C). The cloacal membrane
is thus divided into anal (dorsal) and urogenital (ventral) membranes.
The nodal centre of division is the site of the future perineal body, the Colon at birth
functional centre of the perineum.


In the neonate, the colon is typically 66 cm long and averages 1 cm in
width. The caecum is relatively smaller than in the adult; it tapers into
ENTERIC HINDGUT
the vermiform appendix. The ascending colon is shorter in the neonate,
reflecting the shorter lumbar region. The transverse colon is relatively
The development of the large intestine, whether derived from mid or long, whereas the descending colon is short, but twice the length of the
hindgut, seems to be similar. The proximal end of the colon can be first ascending colon (see Fig. 14.6B). The sigmoid colon may be as long as
identified at stage 15, when an enlargement of a local portion of gut the transverse colon; it often touches the inferior part of the anterior
on the caudal limb of the midgut loop defines the developing caecum. body wall on the left and, in about half of neonates, part of the sigmoid
An evagination of the distal portion of the caecum forms the vermiform colon lies in the right iliac fossa. The muscularis, including the taeniae
appendix at stage 17 (see Fig. 60.3E). Apart from the embryonic studies coli, is poorly developed in the colon, as it is in the small intestine.
of Streeter (1942), there is little information about the development of Appendices, epiploicae and haustra are not present, which gives a
the large intestine in humans. The early endodermal lining of the colon smooth external appearance to the colon. Haustra appear within the
appears stratified, and mitoses occur throughout the layers. A series of first 6 months. The rectum is relatively long; its junction with the anal
longitudinal folds arise initially at the rectum and caecum, and later in canal forms at nearly a right angle.
the regions of colon between these two points. The folds segment into
villi with new villi forming between. The developing mucosa invagi
nates into the underlying mesenchyme between the villi to form glands ANAL CANAL
that increase in number by splitting longitudinally from the base
upwards. The villi gradually diminish in size and are absent by the time Mesenchymal proliferation occurs around the rim of the ectodermal


of birth. aspect of the anal membrane, which thus comes to lie at the bottom


DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE
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of a depression, the proctodeum (see Fig. 72.7E). With the absorption clear whether these cells migrate in from distant sources or differentiate
and disappearance of the anal membrane, the anorectum communi from the investing mesenchyme. The endodermal epithelium overlying
cates with the exterior. The lower part of the anal canal is formed from the lymphoid aggregates is often distorted into a dome shape. The cells
the proctodeal ectoderm and underlying mesenchyme, but its upper within the dome are a mixed population of enterocytes, endocrine cells,
part is lined by endoderm. The line of union corresponds with the goblet cells and M cells. M cells are specialized to provide a mechanism
edges of the anal valves in the adult. The dual origin of the anal canal for the transport of microorganisms and intact macromolecules across
is reflected in its innervation: the endodermal portion is innervated by the epithelium to the intraepithelial space and lamina propria. They
autonomic nerves, and the ectodermal proctodeum is innervated by have been observed in the fetus by 17 weeks; it is believed that they are
spinal nerves. formed by a specialized epithelial–mesenchymal interaction of the
In the fourth and fifth weeks, a small part of the hindgut, the post endoderm and underlying lymphoidtype mesenchyme.
anal gut, projects caudally beyond the anal membrane (see Fig. 60.3B); There are similarly specialized epithelial cells between the entero
it usually disappears before the end of the fifth week. cytes. Intraepithelial leukocytes typically account for 15% of the epithe
Imperforate anus is a term used to describe many different anorectal lial cells of the gut in the adult. They have been observed at 11 weeks,
anomalies. The most common is anal agenesis, which is found in with a distribution of 2–3 intraepithelial leukocytes per 100 gut epithe


almost half of all cases of imperforate anus. The condition is usually lial cells. Both T and B lymphocytes have been described in the develop
associated with a fistula, which opens into the vulva (females) or into ing gut wall. For an account of the development of the immune cells
the urethra (males). It is more rare for the anal membrane to fail to of the gut, consult Butzner and Befus (1989). The neonatal gut becomes
perforate. The condition cannot reliably be diagnosed prenatally by colonized by a range of bacterial flora; some of these exist in a symbiotic
ultrasound diagnosis, and it may be confused with Hirschsprung’s relationship with their host, and some of them may be considered
disease (see below) and colonic atresia. The prognosis is good for low pathogenic.
lesions of the anal canal. The principal concern, in all cases, is the
degree of bowel control, urinary control and, in some cases, sexual
ULTRASOUND ANTENATAL IMAGING OF
function, which is compromised by the condition. Anorectal anomalies
may be indicators of other anomalies, e.g. those forming the ‘VATER’ THE FETAL GUT
syndrome (vertebral, anal, tracheooesophageal and renal anomalies).
The abdominal circumference, routinely estimated at 20 weeks, is cal
culated from the anteroposterior diameter and the transverse abdomi
ENTERIC NERVOUS SYSTEM nal diameter perpendicular to it, taken at the widest part of the
abdomen. The section usually includes one entire rib and the stomach
Enteric neurones are derived from cranial (vagal) neural crest cells at cavity (termed stomach bubble) and can be confirmed on the left side
somite levels 1–7 and from 28 onwards (see Fig. 17.19 and p. 251). of the body (see Fig 14.4G). Anteriorly, the connection of the umbilical
After neurulation, the crest cells begin their ventral migration and invade cord can be confirmed (see Fig 14.4H). Anomalies of the anterior body
the gut via the dorsal mesentery (see Fig. 17.11). Glial cells associated wall, exomphalos and gastroschisis, are readily detected. In exompha


with the gut have been identified as arising from similar levels. It is los, a mass of peritoneal organs herniate through the base of the umbili
thought that the vagal and sacral neural crest cells have intrinsic differ cal ring; in gastroschisis, loops of small intestine and colon float free
ences in their ability to colonize the gut. The local splanchnopleuric in the amniotic fluid (see Fig. 14.5B) (Ionescu 2014).
mesenchyme patterns the crest cells, such that those that enter the gut
layers attain an enteric fate, whereas those that remain outside the gut
FUNCTIONAL MATURITY OF THE GUT AT BIRTH
become committed as parasympathetic postganglionic neurones. The
enteric neurones also migrate to the glands of the gut, e.g. the pancreas.
Migrating vagal neural crest cells reach the midgut by week 5 and the The postnatal maturation of the gut is dependent on the establishment
entire length of the gut is colonized by week 7. Maturation of the of an intestinal microbiota, which, in turn, is affected by gestational
myenteric plexus follows a craniocaudal progression. The submucosal age, mode of delivery, type of feeding and any medical interventions.
plexus arises from centripetally migrating cells from the myenteric plexus In cases of chorioamnionitis, preterm infants ingest bacterial products
2–3 days later (Burns et al 2009). Interstitial cells of Cajal, which derive from the amniotic fluid; it has been suggested that this may be associ
from splanchnopleuric mesenchyme, do not mature in a craniocaudal ated with preterm labour (Neu and Mai 2012). Normal, term, vaginal
progression. They are seen around the myenteric ganglia along the entire delivery establishes the initial colonization of the neonatal gut with
gut from weeks 12–14 (Burns et al 2009). There is evidence that mucosal maternal vaginal and intestinal flora. Twoway interactions between
enteric glial cells, which move into the mucosa after birth, interact with enteric microbes in a biofilm within the luminal glycocalyx of entero


the colonizing intestinal flora, suggesting a microbiotadriven homeo cytes modify intestinal permeability, increase T and B lymphocyte
static mechanism for gut function (Kabouridis et al 2015). numbers within the mucosal lamina propria and mesenteric lymph
nodes, and stimulate postnatal immune development (Vaarala 2012,
Wynn and Neu 2012, Martin et al 2012, Patel et al 2012, Gritz and
Hirschsprung’s disease
Bhandari 2015). Delivery by caesarean section results in the establish
ment of skin microbiota, different intestinal microbes and low micro
Hirschsprung’s disease (commonly called megacolon) is usually charac biota diversity. Failure to develop an appropriate, dynamic, microbiota
terized by an aganglionic portion of gut that does not display peristalsis, is thought to be associated with allergic and inflammatory conditions
and a dilated segment of structurally normal colon proximal to this site. in later life (Wynn and Neu 2012). (For further reading, see Neu (2012),
Histologically, there is either an absence or a reduction in the number Bäckhed et al (2015), Rodríguez et al (2015).)
of ganglia and postganglionic neurones in the myenteric plexus of the The onset of feeding also contributes to gut maturity. Breast milk is
affected segment of gut; postganglionic innervation of the muscle layers a source of epidermal growth factor, which promotes postnatal mucosal
is also often defective. It is believed that the condition is caused by a development and helps mucosal repair. Breast feeding also affects the
failure of neural crest cells to colonize the gut wall appropriately production of immunoglobulin A (IgA) in the gut mucosa (Vaarala
(Gershon 2010). A variable length of large intestine may be affected; the 2012). Undernutrition leads to villous atrophy and, in the preterm
lower and midrectum are the most common sites but, in severe cases, infant, parenteral nutrition is associated with changes in intestinal
the rectum, sigmoid, descending and even proximal colon can be agan structure and function that may lead to increased intestinal permeabil


glionic. Occasionally, aganglionosis affects only a very short length of ity (Martin et al 2012). Antibiotic therapy within the neonatal period
rectum proximal to the anorectal junction and the degree of functional can lead to changes in, and the establishment of, the normal intestinal
obstruction is minimal; in these cases of ‘ultrashortsegment Hirschs microbiota (Martin et al 2012).
prung’s disease’, clinical anomalies arise later in life. Infants with Hir The first passage of faeces of the newborn is termed meconium. This
schsprung’s disease show delay in the passage of meconium, constipation, is a dark, sticky, viscid substance formed from the passage of amniotic
vomiting and abdominal distension. fluid, sloughed mucosal cells, digestive enzymes and bile salts along the
fetal gut. Meconium becomes increasingly solid as gestation advances
but does not usually pass out of the fetal body while in utero. Fetal
GUT-ASSOCIATED LYMPHOID TISSUE distress produced by anoxia may induce the premature defecation of
meconium into the amniotic fluid, with the risk of its inhalation. At
Individual lymphocytes appear in the lamina propria of the gut from birth, the colon contains 60–200 g of meconium. The majority of
approximately week 12 of development, and lymphoid aggregates – neonates defecate within the first 24 hours after birth. Delayed passage
Peyer’s patches – have been noted between 15 and 20 weeks; it is not of stool beyond this time is associated with Hirschsprung’s disease (see


Peritoneal cavity
1059
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above) or imperforate anus. The normal passage of meconium contin Mesenteries of the developing gut
ues for the first 2 or 3 days after birth, and is followed by a transition
to faecal stools by day 7.
The cervicothoracic oesophagus develops between the pericardioperito
neal canals. It is encased in prevertebral, retrotracheal and retrocardiac
mesenchyme. As the pericardioperitoneal canals expand with the devel
PERITONEAL CAVITY oping lung buds, and the diaphragm forms immediately below them;
the oesophagus, at this level, has no true dorsal or ventral mesentery.
The early development of the intraembryonic coelom, which gives rise At superior and intermediate thoracic levels, parts of the lateral aspects
to the peritoneal cavity, is described on page 185. Figure 12.2 shows a of the oesophagus are closely related to the secondary, mediastinal,
scheme of the shape of the early peritoneal cavity and indicates the parietal pleura. In the lower thorax, the oesophagus inclines ventrally
mesenchymal populations derived from its epithelial walls. Initially, the anterior to the descending thoracic aorta. The dorsocaudally sloping
peritoneal cavity associated with the lower end of the foregut has sepa midline diaphragm between oesophageal and aortic orifices may be
rate right and left components: the pleuroperitoneal canals (see Fig. homologized with part of a dorsal mesooesophagus, and is used in
60.1). At the level of the midgut, the pleuroperitoneal canals join a that context in descriptions of diaphragmatic development. A ventral
confluent cavity surrounding the developing gut, which transitorily is midline diaphragmatic strip may also be considered to be a derivative
in communication with the extraembryonic coelom. of a ventral mesooesophagus; however, this region is more usually
The description of the development of the peritoneal cavity that thought of as septum transversum.
follows pertains to changes that occur as a consequence of the differ The alimentary tube, from the diaphragm to the start of the rectum,


ential growth of the gut. initially possesses a sagittal dorsal mesentery. Its line of continuity with
the dorsal parietal peritoneum (i.e. its ‘root’ or ‘line of reflection’) is,
initially, also midline.
The abdominal foregut, from the diaphragm to the future hepato
PERITONEUM
pancreatic duodenal papilla, also has a ventral mesentery. This extends
from the ventrolateral margins of the abdominal oesophagus and as yet
Peritoneum develops from a specific portion of the intraembryonic
‘unrotated’ primitive stomach and proximal duodenum, cranially to the
coelomic walls. Initially, the intraembryonic coelomic epithelium is a
future diaphragm and anteriorly to the ventral abdominal wall (to the
pseudostratified germinal layer from which cellular progeny with dif
level of the cranial rim of the umbilicus). Caudally, between umbilicus
ferent fates arise in specific sites and at specific developmental times.
and duodenum, it presents a crescentic free border.
The portion that will give rise to the peritoneum is derived from the
The midgut and hindgut have no ventral mesentery; thus, the pleural
lower portion of the pericardioperitoneal canals and the somatopleure
and supraumbilical peritoneal cavities are, initially and transiently,
and splanchnopleure associated with the lower foregut, midgut and
bilaterally symmetrical above the umbilicus. Below the umbilicus, the
upper portions of the hindgut (see Figs 12.2, 60.1).
peritoneal cavity is freely continuous across the midline ventral to the
The proliferative splanchnopleuric epithelium produces cell popula
gut (see Fig. 60.5A).
tions for the mucosa and muscularis of the gut, and also for the lamina
propria and epithelium of the visceral peritoneum (the serosa of the Foregut mesenteries
gut wall). The somatopleuric epithelium gives rise to the lamina propria
and epithelium of the parietal peritoneum. The visceral and parietal


The ventral and dorsal foregut mesenteries are relatively large compared
peritoneal layers constitute a mesothelium, which denotes their origin
with the slender endodermal tubes they encase; they are composed
from the intraembryonic mesoderm of the coelomic wall.
of mesenchyme sandwiched between two layers of splanchnopleuric
As the gut grows, splanchnic mesenchyme accumulates around the
coelomic epithelium. A complex series of recesses develop in the
endodermal epithelium and the whole unit generally moves ventrally.
splanchnopleuric mesenchyme and become confluent. As a result of
There is a concomitant enlargement of the caudal ends of the develop
foregut rotation, differential growth of the stomach, liver, pancreas
ing pericardioperitoneal (pleuroperitoneal) canals and developing peri
and spleen, and the completion of the diaphragm, the territories of
toneal cavity. The medial walls of the intraembryonic coelom move
the greater sac and lesser sac (omental bursa) are delimited, and the
closer and there is a relative decrease in the mesenchyme between them.
mesenteric complexes of these organs (omenta and ‘ligaments’) are
The regions where the medial portions of the intraembryonic coelom
defined (see Figs 60.6–60.7).
come together are termed mesenteries. They are composed of two layers
of peritoneum with intervening mesenchyme and contain the neuro
Consequences of rotation of the stomach
vascular structures that pass to and from the gut. At the caudal ends of
the pleuroperitoneal canals, the gut has both ventral and dorsal
mesenteries, whereas, caudal to this, there is only a dorsal mesentery A number of processes occur concurrently, which, conceptually, can be
(see Fig. 60.6; Fig. 60.7). visualized as the movement of the right pleuroperitoneal canal to a
The mesenteries attached to the gut lengthen to permit large move position posterior to the stomach, such that its communication with
ments or rotations of the gut tube. Later, when part or the whole of the the remainder of the peritoneal cavity is reduced. These processes


mesentery lies against the parietal peritoneum, their apposed surfaces include the differential growth of the walls of the stomach, the forma
fuse and are absorbed, i.e. they become sessile. Only those viscera tion and specific local extension of the omenta (dorsal and ventral
developed in direct apposition to one of the primary coelomic regions, mesogastria), and the growth of the liver and, particularly, of the vessels
or a secondary extension of the latter, retain a partial or almost com and ducts that enter and leave the liver. These developments permit
plete visceral serous cover. Thus, the original line of reflection of stomach expansion both anteriorly and posteriorly when food is
mesenteries becomes altered, or, in some cases, the organ may become ingested, and free movement of peristalsis. The right pleuroperitoneal
retroperitoneal. These mechanisms are significant throughout the sub canal forms a discrete region of the peritoneal cavity, the lesser sac, and
diaphragmatic gut, but are predominant in the small and large intestine. the remaining left pleuroperitoneal canal and the remainder of the
All serous membranes may vary their thickness, lines of reflection, peritoneal cavity form the greater sac. The entrance to the original right
disposition, ‘space’ enclosed and their channels of communication, by pleuroperitoneal canal (lesser sac) becomes reduced in size. It is called
a process of areal and thickness growth on one aspect, combined with the epiploic foramen, foramen of Winslow, or the aditus of the omental
cavitation (leading to expanding embryonic recess formation) on the bursa (bursa omentalis).
other.
Early stages of lesser sac development
Although all of the gut tube and its derived glands are associated
with mesenteries formed as described above, the nomenclature for
some portions of the gut and glands is different. Thus, the mesenteries The lesser sac is first indicated by the appearance of multiple clefts
of the stomach are called omenta and the reflections of peritoneum in the paraoesophageal mesenchyme on both left and right aspects
around the liver, which develop from a confluence of splanchnopleuric, of the oesophagus. Although they may become confluent, the left clefts


somatopleuric and septum transversumderived portions, are called are transitory and soon atrophy. The right clefts merge to form the
ligaments. right pneumatoenteric recess that extends from the oesophageal end of
The movements of the developing viscera within the peritoneal the lesser curvature of the stomach as far as the caudal aspect of the
cavity occur with associated movements of the mesothelia that sur right lung bud. At its gastric end, it communicates with the general
round them. The descriptions of peritoneal cavity development that peritoneal cavity and lies ventrolateral to the gut; more rostrally it
follow are thus describing a sequence of changes that affect a complex lies directly lateral to the oesophagus. It is not, as commonly stated,
space and its boundaries. a simple progressive excavation of the right side of the dorsal


DEvEloPmEnT of THE PERiTonEAl CAviTy, gAsTRoinTEsTinAl TRACT AnD iTs ADnExAE
1060
8
noiTCEs
A(i) A(ii)
Oesophagus
Extends cranially into pneumatoenteric recess
Right lung bud
Right pneumatoenteric recess Hepatoenteric Parietal
recess (lesser Inferior vena cava peritoneum
Inferior vena cava in caval fold omental recess)
in caval fold
Epiploic foramen
Hepatoenteric recess
Perigastric,
retrogastric and
greater omental Secondary dorsal mesogastrium
recesses
Lesser omentum, free border Retrogastric and perigastric recesses
B(i) B(ii)
Kidney
Infracardiac bursa Suprarenal gland Line of fusion
Diaphragm
Pneumatoenteric
recess (caudal part)
Inferior vena cava
Liver (early caudate lobe)
Caval fold
Spleen
Hepatoenteric recess
Stomach Spleen
Pancreaticoenteric recess
Pancreas (body) Stomach
C(i) C(ii)
Upper part of lesser sac:
pneumatoenteric and
hepatoenteric regions, Prerenal, retroperitoneal, body of pancreas Kidney
covered by lesser omentum
Entrance via epiploic
foramen and canal
Junction between upper
and lower parts of lesser sac
Lesser omentum Gastrosplenic ligament
Tail of pancreas in splenorenal ligament
Lower part of lesser sac: perigastric,
retrogastric and greater omental
D Lesser omentum Diaphragm E
Liver Aorta
Liver Gastrosplenic ligament
Spleen
Falciform ligament
Splenorenal ligament
Gallbladder
Pancreas
(body)
Entrance to early
epiploic foramen Expanding greater omentum
Fig. 60.7 A–C, Stages of development of the subdiaphragmatic foregut and the right and left pericardioperitoneal/pleuroperitoneal canals, with particular