c h a p t e r
10
Body Cavities
Formation of the Intraembryonic
Cavity
At the end of the third week, intraembryonic
mesoderm on each side of the midline differentiates
into a paraxial portion, an intermediate portion,
and a lateral plate (Fig. 10.1A). When intercellular
clefts appear in the lateral mesoderm, the plates are
divided into two layers: the somatic mesoderm layer
and the splanchnic mesoderm layer. The latter is continuous with mesoderm of the wall of the yolk sac
(Fig. 10.1B). The space bordered by these layers forms the
intraembryonic cavity (body cavity).
At first the right and left sides of the intraembryonic
cavity are in open connection with the extraembryonic cavity, but
when the body of the embryo folds cephalocaudally and laterally,
this connection is lost (Figs. 10.2, A–E). In this manner a large
intraembryonic cavity extending from the thoracic to the pelvic
region forms.
CLINICAL CORRELATES
Body Wall Defects
Ventral body wall defects in the thorax or abdomen may involve the
heart, abdominal viscera, and urogenital organs. They may be due to
a failure of body folding, in which case one or more of the four folds
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Part Two: Special Embryology
Paraxial
mesoderm
Somatic
mesoderm
layer
Intermediate
mesoderm
Intercellular
clefts
Lateral
plate
A
Serous
membrane
Endoderm
B
Wall of
amniotic cavity
Splanchnic
mesoderm
layer
Intraembryonic
cavity
Wall of
yolk sac
Figure 10.1 A. Transverse section through an embryo of approximately 19 days. Intercellular clefts are visible in the lateral plate mesoderm. B. Section through an embryo of
approximately 20 days. The lateral plate is divided into somatic and splanchnic mesoderm layers that line the intraembryonic coelom. Tissue bordering the intraembryonic
coelom differentiates into serous membranes.
(cephalic, caudal, and two lateral) responsible for closing the ventral body wall
at the umbilicus fail to progress to that region. Another cause of these defects
is incomplete development of body wall structures, including muscle, bone,
and skin.
Cleft sternum is a ventral body wall defect that results from lack of fusion
of the bilateral bars of mesoderm responsible for formation of this structure. In
some cases the heart protrudes through a sternal defect (either cleft sternum
or absence of the lower third of the sternum) and lies outside the body (ectopia cordis) (Fig. 10.3A). Sometimes the defect involves both the thorax and
abdomen, creating a spectrum of abnormalities known as Cantrell pentalogy, which includes cleft sternum, ectopia cordis, omphalocele, diaphragmatic
hernia (anterior portion), and congenital heart defects (ventricular septal defect, tetralogy of Fallot). Ectopia cordis defects appear to be due to a failure of
progression of cephalic and lateral folds.
Omphalocele (Fig. 10.3B) is herniation of abdominal viscera through
an enlarged umbilical ring. The viscera, which may include liver, small and
large intestines, stomach, spleen, or bladder, are covered by amnion. The
origin of omphalocele is a failure of the bowel to return to the body cavity
from its physiological herniation during the 6th to 10th weeks. Omphalocele,
which occurs in 2.5/10,000 births, is associated with a high rate of mortality
(25%) and severe malformations, such as cardiac anomalies (50%) and neural
tube defects (40%). Chromosomal abnormalities are present in approximately
50% of liveborn infants with omphalocele.
Gastroschisis (Fig. 10.3C ) is a herniation of abdominal contents through
the body wall directly into the amniotic cavity. It occurs lateral to the umbilicus,
Chapter 10: Body Cavities
Amniotic cavity
213
Surface ectoderm
Somatic
mesoderm
Splanchnic
mesoderm Yolk sac
A
Connection
between
gut and yolk sac
B
Intraembryonic
body cavity
Dorsal
Gut mesentery
C
Figure 10.2 Transverse sections through embryos at various stages of development.
A. The intraembryonic cavity is in open communication with the extraembryonic cavity.
B. The intraembryonic cavity is about to lose contact with the extraembryonic cavity. C.
At the end of the fourth week, splanchnic mesoderm layers are continuous with somatic
layers as a double-layered membrane, the dorsal mesentery. Dorsal mesentery extends
from the caudal limit of the foregut to the end of the hindgut. D and E. Scanning electron
micrographs of sections through mouse embryos showing details similar to those in B
and C, respectively. G, Gut tube; arrowheads, splanchnic mesoderm; C, body cavity;
arrow, dorsal mesentery; A, dorsal aorta; NT, neural tube.
usually on the right, through a region weakened by regression of the right umbilical vein, which normally disappears. Viscera are not covered by peritoneum
or amnion, and the bowel may be damaged by exposure to amniotic fluid.
Both omphalocele and gastroschisis result in elevated levels of α-fetoprotein
in the amniotic fluid, which can be detected prenatally.
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Part Two: Special Embryology
Heart
A
B
C
D
Figure 10.3 Ventral body wall defects. A. Infant with ectopia cordis. Mesoderm of the
sternum has failed to fuse, and the heart lies outside of the body. B. Omphalocele
with failure of the intestinal loops to return to the body cavity following physiological
herniation. The herniated loops are covered by amnion. C. Omphalocele in a newborn.
D. A newborn with gastroschisis. Loops of bowel return to the body cavity but herniate
again through the body wall, usually to the right of the umbilicus in the region of the
regressing right umbilical vein. Unlike omphalocele, the defect is not covered by amnion.
Chapter 10: Body Cavities
215
Lung bud
Pleuropericardial
fold
Phrenic
nerve
C
Heart
Common
cardinal
vein
Figure 10.4 A. Scanning electron micrograph showing the ventral view of a mouse
embryo (equivalent to approximately the fourth week in human development). The gut
tube is closing, the anterior and posterior intestinal portals are visible (arrowheads), and
the heart (H) lies in the primitive pleuropericardial cavity (asterisks), which is partially
separated from the abdominal cavity by the septum transversum (arrow). B. Portion of
an embryo at approximately 5 weeks with parts of the body wall and septum transversum
removed to show the pericardioperitoneal canals. Note the size and thickness of the
septum transversum and liver cords penetrating the septum. C. Growth of the lung
buds into the pericardioperitoneal canals. Note the pleuropericardial folds.
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Part Two: Special Embryology
Gastroschisis occurs in 1/10,000 births but is increasing in frequency,
especially among young women, and this increase may be related to cocaine
use. Unlike omphalocele, gastroschisis is not associated with chromosome
abnormalities or other severe defects. Therefore the survival rate is excellent,
although volvulus (rotation of the bowel) resulting in a compromised blood
supply may kill large regions of the intestine and lead to fetal death.
Serous Membranes
Cells of the somatic mesoderm lining the intraembryonic cavity become
mesothelial and form the parietal layer of the serous membranes lining the
outside of the peritoneal, pleural, and pericardial cavities. In a similar manner,
cells of the splanchnic mesoderm layer form the visceral layer of the serous
membranes covering the abdominal organs, lungs, and heart (Fig. 10.1). Visceral and parietal layers are continuous with each other as the dorsal mesentery
(Fig. 10.2, C and E ), which suspends the gut tube in the peritoneal cavity.
Initially this dorsal mesentery is a thick band of mesoderm running continuously from the caudal limit of the foregut to the end of the hindgut.
Ventral mesentery exists only from the caudal foregut to the upper portion
of the duodenum and results from thinning of mesoderm of the septum
transversum (see Chapter 13). These mesenteries are double layers of peritoneum that provide a pathway for blood vessels, nerves, and lymphatics to the
organs.
Diaphragm and Thoracic Cavity
The septum transversum is a thick plate of mesodermal tissue occupying the
space between the thoracic cavity and the stalk of the yolk sac (Fig. 10.4, A
and B). This septum does not separate the thoracic and abdominal cavities
completely but leaves large openings, the pericardioperitoneal canals, on each
side of the foregut (Fig. 10.4B).
When lung buds begin to grow, they expand caudolaterally within the pericardioperitoneal canals (Fig. 10.4C ). As a result of the rapid growth of the lungs,
the pericardioperitoneal canals become too small, and the lungs begin to expand into the mesenchyme of the body wall dorsally, laterally, and ventrally
(Fig. 10.4C ). Ventral and lateral expansion is posterior to the pleuropericardial
folds. At first these folds appear as small ridges projecting into the primitive
undivided thoracic cavity (Fig. 10.4C ). With expansion of the lungs, mesoderm
of the body wall splits into two components (Fig. 10.5): (a) the definitive wall
of the thorax and (b) the pleuropericardial membranes, which are extensions
of the pleuropericardial folds that contain the common cardinal veins and
phrenic nerves. Subsequently, descent of the heart and positional changes of
Chapter 10: Body Cavities
Primitive
pleural
cavity
217
Superior
vena cava
Parietal
pleura
Parietal
pleura
Lung
Visceral
pleura
Pleural
cavity
Fibrous
pericardium
Pleuropericardial
membrane
Phrenic
nerve
Pericardial
cavity
A
B
Figure 10.5 A. Transformation of the pericardioperitoneal canals into the pleural cavities and formation of the pleuropericardial membranes. Note the pleuropericardial folds
containing the common cardinal vein and phrenic nerve. Mesenchyme of the body wall
splits into the pleuropericardial membranes and definitive body wall. B. The thorax after
fusion of the pleuropericardial folds with each other and with the root of the lungs. Note
the position of the phrenic nerve, now in the fibrous pericardium. The right common
cardinal vein has developed into the superior vena cava.
the sinus venosus shift the common cardinal veins toward the midline, and
the pleuropericardial membranes are drawn out in mesentery-like fashion
(Fig. 10.5A). Finally, they fuse with each other and with the root of the lungs,
and the thoracic cavity is divided into the definitive pericardial cavity and two
pleural cavities (Fig. 10.5B). In the adult, the pleuropericardial membranes
form the fibrous pericardium.
Formation of the Diaphragm
Although the pleural cavities are separate from the pericardial cavity, they remain in open communication with the abdominal (peritoneal) cavity, since the
diaphragm is incomplete. During further development, the opening between
the prospective pleural and peritoneal cavities is closed by crescent-shaped
folds, the pleuroperitoneal folds, which project into the caudal end of the
pericardioperitoneal canals (Fig. 10.6A). Gradually the folds extend medially
and ventrally so that by the seventh week they fuse with the mesentery of the
esophagus and with the septum transversum (Fig. 10.6B). Hence the connection between the pleural and peritoneal portions of the body cavity is closed
by the pleuroperitoneal membranes. Further expansion of the pleural cavities
relative to mesenchyme of the body wall adds a peripheral rim to the pleuroperitoneal membranes (Fig. 10.6C ). Once this rim is established, myoblasts
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Part Two: Special Embryology
Pericardioperitoneal
Pleuroperitoneal
fold
Esophagus
mesentery
Aorta
Pleuroperitoneal
membrane
Esophagus
canal
A
B
Septum transversum
Inferior
vena
cava
C
Muscular
ingrowth from
body wall
Septum
transversum
Figure 10.6 Development of the diaphragm. A. Pleuroperitoneal folds appear at the
beginning of the fifth week. B. Pleuroperitoneal folds fuse with the septum transversum
and mesentery of the esophagus in the seventh week, separating the thoracic cavity
from the abdominal cavity. C. Transverse section at the fourth month of development.
An additional rim derived from the body wall forms the most peripheral part of the
diaphragm.
originating in the body wall penetrate the membranes to form the muscular
part of the diaphragm.
Thus the diaphragm is derived from the following structures: (a) the septum
transversum, which forms the central tendon of the diaphragm; (b) the two
pleuroperitoneal membranes; (c) muscular components from the lateral and
dorsal body walls; and (d) the mesentery of the esophagus, in which the crura
of the diaphragm develop (Fig. 10.6C ).
Initially the septum transversum lies opposite cervical somites, and nerve
components of the third, fourth, and fifth cervical segments of the spinal
cord grow into the septum. At first the nerves, known as phrenic nerves, pass
into the septum through the pleuropericardial folds (Fig. 10.4B). This explains
why further expansion of the lungs and descent of the septum shift the phrenic
nerves that innervate the diaphragm into the fibrous pericardium (Fig. 10.5).
Although the septum transversum lies opposite cervical segments during
the fourth week, by the sixth week the developing diaphragm is at the level of
thoracic somites. The repositioning of the diaphragm is caused by rapid growth
of the dorsal part of the embryo (vertebral column), compared with that of the
ventral part. By the beginning of the third month some of the dorsal bands of
the diaphragm originate at the level of the first lumbar vertebra.
The phrenic nerves supply the diaphragm with its motor and sensory innervation. Since the most peripheral part of the diaphragm is derived from
mesenchyme of the thoracic wall, it is generally accepted that some of the
lower intercostal (thoracic) nerves contribute sensory fibers to the peripheral
part of the diaphragm.
Chapter 10: Body Cavities
219
CLINICAL CORRELATES
Diaphragmatic Hernias
A congenital diaphragmatic hernia, one of the more common malformations
in the newborn (1/2000), is most frequently caused by failure of one or both of
the pleuroperitoneal membranes to close the pericardioperitoneal canals. In
that case the peritoneal and pleural cavities are continuous with one another
along the posterior body wall. This hernia allows abdominal viscera to enter
the pleural cavity. In 85 to 90% of cases the hernia is on the left side, and
intestinal loops, stomach, spleen, and part of the liver may enter the thoracic
cavity (Fig. 10.7). The abdominal viscera in the chest push the heart anteriorly
and compress the lungs, which are commonly hypoplastic. A large defect is
associated with a high rate of mortality (75%) from pulmonary hypoplasia
and dysfunction.
Occasionally a small part of the muscular fibers of the diaphragm fails to
develop, and a hernia may remain undiscovered until the child is several years
old. Such a defect, frequently seen in the anterior portion of the diaphragm,
is a parasternal hernia. A small peritoneal sac containing intestinal loops
may enter the chest between the sternal and costal portions of the diaphragm
(Fig. 10.7A).
Another type of diaphragmatic hernia, esophageal hernia, is thought
to be due to congenital shortness of the esophagus. Upper portions of the
stomach are retained in the thorax, and the stomach is constricted at the level
of the diaphragm.
SUMMARY
At the end of the third week, intercellular clefts appear in the mesoderm on
each side of the midline. When these spaces fuse, the intraembryonic cavity
(body cavity), bordered by a somatic mesoderm and a splanchnic mesoderm
layer, is formed (Figs. 10.1 and 10.2). With cephalocaudal and lateral folding of
the embryo, the intraembryonic cavity extends from the thoracic to the pelvic
region. Somatic mesoderm will form the parietal layer of the serous membranes lining the outside of the peritoneal, pleural, and pericardial cavities.
The splanchnic layer will form the visceral layer of the serous membranes
covering the lungs, heart, and abdominal organs. These layers are continuous
at the root of these organs in their cavities (as if a finger were stuck into a
balloon, with the layer surrounding the finger being the splanchnic or visceral
layer and the rest of the balloon, the somatic or parietal layer surrounding the
body cavity). The serous membranes in the abdomen are called peritoneum.
The diaphragm divides the body cavity into the thoracic and peritoneal
cavities. It develops from four components: (a) septum transversum (central
tendon); (b) pleuroperitoneal membranes; (c) dorsal mesentery of the esophagus; and (d) muscular components of the body wall (Fig. 10.6). Congenital
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Part Two: Special Embryology
Opening between sternal
and costal heads
Inferior
vena cava
Central
tendon
Opening for
esophagus
Left lung
Colon
Aortic hiatus
A
Absence of
pleuroperitoneal
membrane
Diaphragm
Stomach
B
C
Figure 10.7 Congenital diaphragmatic hernia. A. Abdominal surface of the diaphragm
showing a large defect of the pleuroperitoneal membrane. B. Hernia of the intestinal
loops and part of the stomach into the left pleural cavity. The heart and mediastinum
are frequently pushed to the right and the left lung compressed. C. Radiograph of a
newborn with a large defect in the left side of the diaphragm. Abdominal viscera have
entered the thorax through the defect.
Chapter 10: Body Cavities
221
diaphragmatic hernias involving a defect of the pleuroperitoneal membrane on
the left side occur frequently.
The thoracic cavity is divided into the pericardial cavity and two pleural
cavities for the lungs by the pleuropericardial membranes (Fig. 10.5).
Double layers of peritoneum form mesenteries that suspend the gut tube
and provide a pathway for vessels, nerves, and lymphatics to the organs. Initially, the gut tube from the caudal end of the foregut to the end of the hindgut is
suspended from the dorsal body wall by dorsal mesentery (Fig. 10.2, C and E ).
Ventral mesentery derived from the septum transversum exists only in the region of the terminal part of the esophagus, the stomach, and upper portion of
the duodenum (see Chapter 13).
Problems to Solve
1. A newborn infant cannot breathe and soon dies. An autopsy reveals a large
diaphragmatic defect on the left side, with the stomach and intestines
occupying the left side of the thorax. Both lungs are severely hypoplastic. What
is the embryological basis for this defect?
2. A child is born with a large defect lateral to the umbilicus. Most of the large
and the small bowel protrude through the defect and are not covered by
amnion. What is the embryological basis for this abnormality, and should you
be concerned that other malformations may be present?
SUGGESTED READING
Cunniff C, Jones KL, Jones MC: Patterns of malformations in children with congenital diaphragmatic
defects. J Pediatr 116:258, 1990.
Puri P, Gormak F: Lethal nonpulmonary anomalies associated with congenital diaphragmatic hernia: implications for early intrauterine surgery. J Pediatr Surg 35:29, 1984.
Skandalakis JE, Gray SW: Embryology for Surgeons: The Embryological Basis for the Treatment of
Congenital Anomalies. 2nd ed. Baltimore, Williams & Wilkins, 1994.