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Pleuroperitoneal Canal Closure and the Fetal Adrenal Gland.

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THE ANATOMICAL RECORD 294:633–644 (2011)
Pleuroperitoneal Canal Closure and the
Fetal Adrenal Gland
SHOGO HAYASHI,1,2* YOSHITAKA FUKUZAWA,1
JOSÉ FRANCISCO RODRÍGUEZ-VÁZQUEZ,3 BAIK HWAN CHO,4
SAMUEL VERDUGO-LÓPEZ,3 GEN MURAKAMI,5 AND TAKASHI NAKANO2
1
Medical Education Center, Aichi Medical University School of Medicine, Nagakute, Japan
2
Department of Anatomy, Aichi Medical University School of Medicine, Nagakute, Japan
3
Departamento de Anatomı́a y Embriologı́a Humana II, Facultad de Medicina,
Universidad Complutense, Madrid, España
4
Department of Surgery, Chonbuk National University School of Medicine, Jeonju, Korea
5
Division of Internal Medicine, Iwamizawa Kojin-kai Hospital, Iwamizawa, Japan
ABSTRACT
Pleuroperitoneal canal (PP canal) closure is generally considered to
result from an increase in the height, and subsequent fusion, of the bilateral pleuroperitoneal folds (PP folds). However, the folds develop in the
area ventral to the adrenal, in contrast to the final position of the diaphragm, which extends to the dorsal side of the adrenal (the ‘‘retro-adrenal’’ diaphragm). We examined the semiserial histology of 20 human
embryos and fetuses (crown-rump length 11–40 mm). We started observations of the canal at the stage through which the lung bud extends far
caudally along the dorsal body wall to the level of the future adrenal, and
the phrenic nerve has already reached the PP fold. Subsequently, the
developing adrenal causes narrowing of the dorsocaudal parts of the
canal, and provides the bilateral midsagittal recesses or ‘‘false’’ bottoms of
the pleural cavity. However, at this stage, the PP fold mesenchymal cells
are still restricted to the ventral side of the adrenal, especially along the
liver and esophagus. Thereafter, in accordance with ascent of the lung,
possibly due to anchoring of the liver to the adrenal, the PP fold mesenchymal cells seem to migrate laterally along the coelomic mesothelium
covering some sheet-like loose mesenchymal tissue behind the adrenal.
Final closure of the PP canal by lateral migration to provide the ‘‘retroadrenal’’ diaphragm is a process quite different from the common dogma.
It is likely that the sheet-like loose mesenchymal tissue becomes the caudal part of the pleural cavity through a process involving cell death. Anat
C 2011 Wiley-Liss, Inc.
Rec, 294:633–644, 2011. V
Key words: pleuroperitoneal canal; adrenal; lung bud; liver;
coelomic mesothelium; human fetus
Closure of the pleuroperitoneal canal (PP canal) is
generally considered to result from an increase in the
height and thickness, and even fusion, of the bilateral
pleuroperitoneal folds (PP folds) containing the muscle
precursors of the diaphragm (Hamilton and Mossman,
1978). According to some textbooks (e.g., Gray’s Anatomy; Collins, 2005), the bilateral pleural cavities extend
into the mesenchyme on the ‘‘dorsal’’ side of the adrenal
glands, the gonads and the mesonephric ridges. Thus,
conversely, the PP canal is likely to be closed by the
fusion of its edges, through growth of the organs
C 2011 WILEY-LISS, INC.
V
Grant sponsor: Ministry of Health and Welfare (R & D
program for Cancer Control), Republic of Korea; Grant number:
0620220-1.
*Correspondence to: Shogo Hayashi, MD, PhD, Medical Education Center, Aichi University School of Medicine, Nagakute,
Aichi 480-1195, Japan. Fax: þ81-561-63-1037. E-mail: shogo@
aichi-med-u.ac.jp
Received 28 May 2010; Accepted 21 December 2010
DOI 10.1002/ar.21351
Published online 2 March 2011 in Wiley Online Library
(wileyonlinelibrary.com).
634
HAYASHI ET AL.
surrounding it, particularly that of the adrenal glands.
However, as the fold develops in areas far cranioventral
to the adrenal, i.e., those surrounded by the heart, liver,
and cranial parts of the lung bud, does the PP fold really
extend dorsocaudally to the dorsal side of the adrenal?
Moreover, to our knowledge, the timing of closure of the
PP canal has not yet been demonstrated in photographs.
Botha (1959) has already provided a limited clue, as he
reported that the PP canal is still widely open at the embryonic 12-mm stage and that muscle tissue extends
into the membrane, which appears to close completely
the canal at the 17.5-mm stage. Unfortunately, Botha
did not demonstrate a sequence for the closure process,
as this was beyond the scope of his study. Consequently,
the aim of the present study was to re-examine the process of PP canal closure using semiserial sections of
human embryos or fetuses.
MATERIALS AND METHODS
The study was performed in accordance with the provisions of the Declaration of Helsinki 1995 (as revised in
Edinburgh 2000). We examined the paraffin-embedded
histology of 20 embryos or fetuses [crown-rump length
(CRL) 11–40 mm] at 6–12 weeks of gestation. However,
as there was a possibility that estimates of ovulational
age (coital age) might have been mixed with estimates
based on the week of pregnancy, we classified these
specimens into three groups according to the size: seven
specimens with CRL 11–13 mm (early stage group),
eight specimens with CRL 16–23 mm (mid-stage group),
and five specimens with CRL 28–40 mm (late-stage
group). All the specimens were part of the large collection kept at the Embryology Institute of the Universidad
Complutense, Madrid, and were the products of miscarriages and ectopic pregnancies at the Department of Obstetrics of the University. Approval for the study was
granted by the university ethics committee. Because of
the nature of the specimens, we were unable to rule out
the presence of pathology, but our aim was to describe
the morphology that was commonly evident in each of
the early, mid- and late-stage groups.
After routine procedures for paraffin-embedded histology, most of the specimens were cut horizontally, and
four sagittally (one specimen with CRL 19 mm; two with
CRL 20 mm; one with CRL 21 mm) with a thickness of 5
lm, at intervals of 20 lm. Approximately 100–200 sections were prepared for each specimen, and all sections
were stained with hematoxylin and eosin.
RESULTS
Early Stage Group (CRL 11–13 mm, Seven
Specimens)
The PP canal was identified as an irregularly shaped
space surrounded by the liver, esophagus, mesonephros,
and the so-called PP fold (Figs. 1–3). Likewise, through
a narrow potential space between the lateral body wall
and liver surface, the abdominal and thoracic parts of
the coelomic cavity were connected (Figs. 1E, 2F, and
3F). This space was also included in the PP canal. The
bilateral lung buds were surrounded by the liver from
the ventral aspect, and not located on the cranial side of
the liver, as is the case in adults (Fig. 1). Through the
PP canal, the lung bud extended far caudally from the
dorsal side of the heart, along the dorsal body wall, to
the level of the future adrenal (Figs. 1–3). At this stage,
the phrenic nerve had already reached the PP fold (Fig.
1A–C).
In two of the seven early stage specimens (both, CRL
11 mm; Fig. 1), the mesonephros did not yet accompany
the adrenal and was located closely to and facing the
ventrally located PP fold. Most of the PP fold mesenchymal cells were restricted to the area between the heart
and liver, especially along the dorsal aspect of the liver,
but some of the cells formed a fold connecting to the dorsal body wall (Fig. 1C). In five specimens (Figs. 2 and 3),
the mesonephros was attached to the lateral aspect of
the adrenal. Moreover, the right adrenal was fused with
the right lobe of the liver to provide a route for the
future inferior vena cava (we have described the process
of venous communication in another article: Jin et al.,
2010). Thus, in these five specimens, the liver was anchored to the dorsal abdominal wall via the right adrenal.
The PP fold mesenchymal cells were identified along the
dorsal aspect of the liver, including a site close to the
liver-adrenal fusion, and alongside the esophagus.
The developing adrenal gland caused narrowing of the
dorsocaudal part of the PP canal. During this process,
bilateral ‘‘paramedian recesses’’ (blind sacs) of the PP
canal or coelomic cavity were formed immediately caudal
to the lung bud (Figs. 2E,F and 3D–F), being located
between the bilateral adrenals and attached to them.
These recesses appeared to form the ‘‘bottoms’’ of the
canal, creating an impression that the primitive pleural
cavity ended on or near the adrenal. However, the PP
canal was still open bilaterally alongside the posterolateral surface of the liver, especially between the liver and
the mesonephros, despite the fact that, at the craniolateral ends, the PP fold connected with the lateral coelomic mesothelium (Fig. 3A). Thus, the adrenal did not
close the PP canal.
Consistently on the right side (Fig. 1E) and often on
both sides (three of the seven specimens; Figs. 2D and
3C,D), the esophagus accompanied a recess or recesses
of the coelomic cavity (the pneumatoenteric recess
described by Kanagasuntheram, 1957). The pneumatoenteric recess opened or communicated with the PP canal
in the cranial part, whereas the right recess continued
to the developing lesser sac at the caudal end. Thus, the
right recess contained the developing caudate lobe of the
liver (we have described the detailed morphology in
another article: Hwang et al., 2010). The bilateral lung
buds carried free caudal ends without a mesentery-like
structure connecting to the esophagus (Figs. 1E, 2D, and
3C). On the dorsal side of the lung bud, thick, loose,
sheet-like mesenchymal tissue was present along the
dorsal body wall (Figs. 2 and 3). This sheet-like structure was covered by the coelomic epithelium. Notably, in
four of the seven early stage specimens (CRL 11 or 13
mm), the PP fold connected with the covering mesothelium at the level of the heart apex (Figs. 2A,B and 3A).
Mid-Stage Group (CRL 16–23 mm, Eight
Specimens)
In this group, we found several critical events involved
in closure of the PP canal. However, the larger specimens did not always show the hypothetical later step of
sequential events. One of the striking differences
HUMAN PLEUROPERITONEAL CANAL CLOSURE
635
Fig. 1. Pleuroperitoneal canal opens in the caudal side: an 11-mm
CRL-embryo. Horizontal sections. Hematoxylin and eosin (HE) staining. The right-hand side of the figure corresponds to the right side of
the body. A: (E) is the most cranial (caudal) level in this figure. A: displays a lower magnification view, whereas B, C, D, and E are prepared at the same magnification (scale bars in A and B). The
pleuroperitoneal canal is a narrow space surrounded by the bilateral
lung buds (LB), the pleuroperitoneal fold (PPF), the mesonephros
(MN), and the esophagus (E). In this specimen, the canal gives off two
recess-like structures in A and C (open stars), but they open in the
caudal side (B and D). The pericardial cavity (PCC) is closed in A. The
phrenic nerve has already reached the caudal part of the PPF (arrows
in A–C). E shows caudal ends of the lung bud without mesentery-like
structure: the left end is caudal to the right one in this specimen. In E,
the esophagus accompanies the pneumatoenteric recess of the coelomic cavity (black stars in D and E). The most lateral and caudal parts
of the pleuroperitoneal canal are indicated by open circles in E. At any
level, the liver (L) is still separated from the dorsal body wall by the
coelomic cavity. AO, aorta; DV, ductus venosus; PCV, posterior cardinal vein.
between this stage, and the early stage was in the topographical anatomy of the lung, adrenal, and diaphragm.
The developing lung ascended to occupy a final position
alongside almost the entire craniocaudal extent of the
heart. Thus, the lung disappeared from the craniocaudal
level of the adrenal (Fig. 4; CRL 17 mm). However, as
seen in Fig. 5 (CRL 23 mm), the caudal end of the lung
bud still remained at the level of the adrenal. In a specimen with CRL 19 mm (Fig. 6), the lung was located far
cranial to the adrenal.
636
HAYASHI ET AL.
Fig. 2. Pleuroperitoneal fold mesenchyme contributes to the liver
fusion with the right adrenal: a 13-mm CRL-embryo. Horizontal sections. HE staining. The right-hand side of the figure corresponds to
the right side of the body. A: (F) is the most cranial (caudal) level in
this figure. The pleuroperitoneal fold (PPF), containing dense mesenchymal tissues (asterisks), separates the liver (L) from the heart (H in
A) and from the lung bud (LB in B). However, in C and D, the fold
does not attach to the body wall, but the dense mesenchyme (asterisks) is restricted along the dorsal aspect of the liver near the esophagus (E). The dense mesenchyme contributes to fusion of the adrenal
(AD) with the liver in E and F, but the inferior vena cava has not yet
formed. The caudal part of the pleuroperitoneal canal makes the
recess or blind sac attaching to the adrenal (open stars, E and F). The
pneumatoenteric recess is seen in C–E (black stars). The left lung end
is caudal to the right one in this specimen. Note a thick sheet of loose
mesenchymal tissues (SLMT) in the dorsal and lateral sides of the
lung bud. The most lateral and caudal part of the pleuroperitoneal
canal is indicated by open circles in F. All panels are prepared at the
same magnification (scale bar in A). AO, aorta; GC, gastric cardia;
MN, mesonephros; PCV, posterior cardinal vein.
The PP canal was closed by the diaphragm extending
‘‘behind’’ the adrenal. Within the developmental period
between the early and mid stages, the PP fold mesenchymal cells appeared to reach the dorsal site immediately ventral to the abdominal aorta. As seen in Fig. 4,
the PP fold mesenchymal cells were concentrated near
the esophagus and appeared to be undergoing lateral
migration along the coelomic mesothelium behind the
adrenal. This mesothelium covered the ventral aspect of
the sheet-like mesenchymal tissue along the dorsal body
HUMAN PLEUROPERITONEAL CANAL CLOSURE
637
Fig. 3. False bottom of the pleural cavity near the adrenal: an 11mm CRL-embryo. A specimen different from that shown in Fig. 1. Horizontal sections. HE staining. The right-hand side of the figure corresponds to the right side of the body. A: (F) is the most cranial (caudal)
level in this figure. The pleuroperitoneal fold (PPF), containing dense
mesenchymal tissues, separates the liver (L) from the heart (H) in A,
but it does not attach to the body wall in B. The fold attaches to the
coelomic mesothelium in the cranial parts (arrows in A). The right lung
end is caudal to the left one in this specimen (C and D). In D, E, and
F, the adrenal (AD) is fused with the liver to provide a route of the inferior vena cava (IVC). The caudal parts of the pleuroperitoneal canal
make the recess or blind sac attaching to the adrenal (open stars, D–
F): they appeared to be the bottom of the pleural cavity, but the pleuroperitoneal canal is not closed. The most lateral and caudal parts of
the pleuroperitoneal canal are indicated by open circles in panel F.
The dense mesenchymal tissues are concentrated near the esophagus
(E) (PPF in C). The pneumatoenteric recess is indicated by black stars
in C–F. Note a thick sheet of loose mesenchymal tissues (SLMT) along
the dorsal body wall. A, B, and F (C–E) are of the same magnification
(scale bars in A and C). AO, aorta; GC, gastric cardia; LB, lung bud;
MN, mesonephros; H, heart; PCV, posterior cardinal vein.
wall (see the final paragraph of the first subsection). The
celiac ganglion of the sympathetic nerve was located immediately caudal to the developing diaphragm. As shown
in Fig. 5, the PP fold mesenchymal cells extended later-
ally to reach the body wall, whereas the sheet-like mesenchymal tissue was reduced in thickness.
The gastric cardia with the spleen, as well as the mesonephros and gonad, were located on the abdominal side
638
HAYASHI ET AL.
Fig. 4. Pleuroperitoneal fold mesenchymal cells migrating along the
mesothelium: a 17-mm CRL-embryo. Horizontal sections. HE staining.
The right-hand side of the figure corresponds to the right side of the
body. A: (C) is the most cranial (caudal) in the figure. B shows the
most caudal part of the pleural cavity (PLC): the pleuroperitoneal canal
was closed in this level. The pleuroperitoneal fold mesenchymal cells
(PPF) are concentrated in a site behind the abdominal esophagus (GC
in A) and between the bilateral adrenals (AD in B). The mesenchymal
cells appear to migrate laterally along the mesothelium covering the
thick sheet of loose mesenchymal tissue (SLMT). Black stars indicate
the developing lesser sac containing the caudate lobe of the liver (CL).
B and C are prepared at the same magnification (scale bars in A and
B). AO, aorta; CG, celiac ganglion; GC, gastric cardia; IVC, inferior
vena cava; L, liver; LGA, left gastric artery; MN, mesonephros.
HUMAN PLEUROPERITONEAL CANAL CLOSURE
Fig. 5. Diaphragm extending behind the adrenal: a 23-mm CRLembryo. Horizontal sections. HE staining. The right-hand side of the
figure corresponds to the right side of the body. A: (C) is the most cranial (caudal) level in this figure. Arrowheads in A, B, and C indicate
attachments of the developing diaphragm to the lateral body wall. D
and F are higher magnification views of the central part of A and C,
respectively. E (the caudal end of the lung) corresponds to an intermediate level between A and B. In A, the caudal parts of the lung bud
(LB) are still located in the level of the liver (L) and right adrenal (AD).
639
The sheet-like loose mesenchymal tissues (SLMT in F) is thin or difficult to identify in A–E. Instead, the pleural cavity (PLC) extends widely
between the dorsal body wall and diaphragm (arrows). In D, the latter
structure contains dense tissues, possibly muscle precursors, near the
esophagus (E). A–C are prepared at the same magnification (scale
bars in A, D, E, and F). AO, aorta; CL, caudate lobe of the liver; DV,
ductus venosus; H, heart; PCV, posterior cardinal vein; E, esophagus;
GC, gastric cardia; IVC, inferior vena cava; SP, spleen.
640
HAYASHI ET AL.
the primitive pleural cavity was located at the level of
the 12th thoracic or first lumbar vertebra (Fig. 6). Most
of this bottom area was covered by the adrenal from the
ventral side. A possible remnant of the PP fold (Fig. 6B)
was evident as a loose tissue band connecting the lung
and diaphragm, being similar to the ligamentum pulmonale in adults. The paramedian recess on or near the adrenal (the false bottom of the pleural cavity) had
disappeared in mid-stage specimens.
Late-Stage Group (CRL 28–40 mm, Five
Specimens)
At this stage, the diaphragm was already situated in
its final position. The right adrenal and liver were separated by loose tissue (Fig. 8). The striated muscle fibers
of the diaphragm were clearly identified near and along
the esophagus. However, muscle fibers did not cross the
ventral aspect of the esophagus. The dome-like cranial
part of the diaphragm, covering the future bare area of
the liver, was still membranous. The sheet-like mesenchymal tissue was reduced in thickness or difficult to
find. Thus, the parietal pleura were located closely to
the rib and intercostal nerve (Fig. 8). The left pneumatoenteric recess had disappeared, whereas the right
recess (parts of the lesser sac) had expanded to contain
the large caudate lobe of the liver.
DISCUSSION
Fig. 6. Muscle fiber distribution in the pleuroperitoneal fold: a 19mm CRL-embryo and a 21-mm CRL-embryo. Sagittal sections. HE
staining. A specimen shown in A, B, C, and D is bit earlier than
another specimen shown in E and F. A (D) is the most rightward (leftward) level in these four panels. The pleuroperitoneal fold extends
along the cranial side of the liver (L) and bilateral adrenals. Muscle
fibers (arrows) are concentrated around the esophagus (E) as well as
in the cranial side of the adrenal (AD) and the caudate lobe of the liver
(CL). In B, a possible remnant of the pleuroperitoneal fold is seen
(asterisks). All panels are prepared at the same magnification (scale
bar in A). AO, aorta; CG, celiac ganglion; DV, ductus venosus; GD,
gonad; H, heart; IVC, inferior vena cava; J, jejunum; K, definite kidney;
LB, lung bud; P, pancreas; PV, portal vein; S, stomach; T, trachea.
of the diaphragm extending behind the adrenal (Figs. 5
and 6). Notably, on both sides of the body, the caudal aspect of the diaphragm was connected tightly with the
mesonephros (Fig. 7). The triangular-shaped bottom of
The present study demonstrated paramedian recesses
at the dorsocaudal part of the PP canal in fetuses with
CRL 11–13 mm. These recesses contained the bilateral
lung buds and ended on or near the developing adrenal.
However, the lateral parts of the PP canal still maintained communication between the thoracic and abdominal parts of the coelomic cavity along the liver surface.
Thus, these paramedian recesses provided false bottoms
for the pleural or thoracic cavity. The bilateral adrenals
did not close the PP canal by acting as obstacles. Likewise, we did not find any direct contribution of the bilateral PP folds to closure of the PP canal, such as fusion
of the crescentric free edges. Such morphology may be
attributable to overinterpretation of fusion between the
mesonephros and PP fold or between the PP fold and
the lateral coelomic mesothelium. Instead, closure of the
PP canal seems to be completed by lateral migration of
the PP fold mesenchymal cells along the coelomic mesothelium behind the adrenal. Figure 9 shows the hypothetical courses of the PP fold mesenchymal cells. In
short, they seem to migrate (1) caudally along the dorsal
aspect of the liver, (2) dorsally along and around the
esophagus, and (3) laterally along the coelomic
mesothelium.
In the early stage, the PP fold was located on the ventral side of the adrenal, gonad, and mesonephros. However, to separate these organs from the future pleural or
thoracic cavity, the diaphragm should extend along the
dorsal side of these abdominal viscera, as is the case for
the adult pleural recesses. The most striking observation
in this study was ‘‘switching’’ from the ventrally located
PP fold to the final, retro-adrenal diaphragm. This event
seems to occur within a short period between the early
and mid stages, that is, at the CRL 13–16-mm stage or
possibly within a few days at an ovulation age of 6
HUMAN PLEUROPERITONEAL CANAL CLOSURE
641
Fig. 7. Diaphragm and mesonephros: a 19-mm CRL-embryo and a
20-mm CRL-embryo. Sagittal sections. HE staining. A and B: 19 mmCRL; C and D: 20-mm CRL. A and C (B and D) display the cranial end of
the right (left) mesonephros (MN).The connective tissues of the meso-
nephros continue to the diaphragm (DIA). The adrenal is located lateral
side of these panels. All panels are prepared at the same magnification
(scale bar in A). CG, celiac ganglion; GC, gastric cardia; GD, gonad; L,
liver; S, stomach.
weeks. The retro-adrenal diaphragm is likely to form
along, or even replace, the coelomic mesothelium covering the loose, dorsal, sheet-like mesenchymal tissue. The
connection between the covering mesothelium and the
PP fold is first evident alongside the heart even at the
CRL 11-mm stage. However, the first connection site
was located ventral, lateral, and far cranial to the adrenal (Figs. 2B and 3A). To approach a site behind the ad-
renal, a caudal course along and around the esophagus
is most likely (Fig. 9). We hypothesize that the sheetlike mesenchymal tissue changes to the most caudal
part of the pleural or thoracic cavity through a mechanism involving cell death. This change seems to be
closely related to another marked change in the topographical relationship between the liver and the lung.
Consequently, in humans, the bilateral PP folds
642
HAYASHI ET AL.
Fig. 8. Final topographical anatomy of the diaphragm: a 35-mm
CRL-fetus. Horizontal sections. HE staining. The right-hand side of the
figure corresponds to the right side of the body. A (D) is the most cranial (caudal) level in this figure. In A and B, the diaphragm (DIA) is
thick with striated muscles near the esophagus (E), whereas the lateral
parts are membranous. A vacant pleural cavity (PLC) in B indicates a
distance between the lung and adrenal. In C and D, the right adrenal
(AD) does not attach to the liver (L) but is separated by a loose tissue
(arrows). In D, the lesser sac (black stars) contains the caudate lobe
of the liver (CL). The mesonephros disappears in these levels. A
sheet-like mesenchymal tissue is difficult to identify (cf. Fig. 4). All
panels are prepared at the same magnification (scale bar in A). AO,
aorta; GC, gastric cardia; ICN, intercostal nerve; IVC, inferior vena
cava; LB, lung bud.
themselves do not seem to fuse together to form a domelike diaphragm.
We speculate that, in addition to the lateral plate mesoderm, the PP fold mesenchymal cells also contribute to
fusion between the liver and the right adrenal in fetuses
at the CRL 11–13 mm stage. Anchoring of the liver to
the right adrenal surface seems to be critically important not only for development of the inferior vena cava
(Jin et al., 2010) but also for ascent of the lung bud from
the level of the adrenal. Without the liver alongside the
heart, in turn, the lung seems to easily occupy in the
future thoracic cavity. In the left side of the body, fusion
between the adrenal and liver seems to be interrupted
by the developing gastric cardia. Thus, conversely, the
PP fold mesenchymal cells seem to simply migrate along
the dorsal aspect of the liver, the esophagus, and the mesothelium covering the sheet-like mesenchymal tissue.
In the late-stage group, the liver and right adrenal were
clearly separated by loose tissue. Thus, the PP fold cells
may play a limited, temporary role in fusion between
the liver and the right adrenal.
Using adult cadavers, Kawada et al. (2007) investigated the histological architecture of the small interface
area between the pleural and peritoneal cavities without
the diaphragm and other striated muscles: this area, or
Bochdalek’s triangle, was consistently located just cranial
to the 12th rib and often behind the kidney. Bochdalek’s
triangle does not seem to correspond to the paramedian
recess near the fetal adrenal but to the triangular-shaped
bottom of the pleural cavity derived from the sheet-like
mesenchymal tissue along the dorsal body wall. This bottom part seems to be uncovered by the definitive adrenal
after birth. Bochdalek’s triangle in the adult may correspond to the site of initial attachment between the PP
fold and the lateral coelomic mesothelium.
Recently, Greer and coworkers have extensively
described the pathogenesis of nitrofen-induced congenital diaphragmatic hernia (CDH) (Clugston et al.,
2010a,b; Clugston and Greer, 2007): Clugston et al.
(2008) identified human genes related to CDH and demonstrated that they are expressed in the nonmuscular,
mesenchymal component of the diaphragm. Thus, CDH
HUMAN PLEUROPERITONEAL CANAL CLOSURE
Fig. 9. Schematic representation showing hypothetical migration
courses of the pleuroperitoneal fold mesenchymal cells. In A, we
superimpose thoracoabdominal structures of stages 11–23-mm CRL
to show sequential migration processes of the pleuroperitoneal fold
mesenchymal cells: (1) along the posterior surface of the liver (L) that
faces the heart (H), (2) along the posterior surface of the liver that
faces the lung bud (LB), (3) toward the dorsal aspect of the esophagus
(E), (4) toward the fusion between the right adrenal (AD) and liver and,
(5) along the mesothelium covering the bilateral sheet-like loose mes-
643
enchymal tissues (SLMT). The Process 5 or lateral migration does not
finally occur but stars early possibly together with the Process 3: it is
first seen at the superior level above the adrenal (see Fig. 2B). The
pleuroperitoneal fold mesenchymal cells are drawn by blue–green belt,
but at a certain stage if limited, they never provide a continuous belt
from the Processes 1–5. B and C are cross sections corresponding to
those Processes 1–2 or 4–5, respectively. The gastric cardia (GC) is
actually located behind the liver, but the former is pulled caudally to
show the Process 5. AO, aorta.
644
HAYASHI ET AL.
has its origins in a mesenchymal defect; Ackerman et al.
(2005) reported that the lung and diaphragm might carry
a common regulator gene such as Fog2, and that the lung
bud is essentially important for enlargement of the canal;
Belik et al. (2003) reported that epithelium-dependent
airway muscle relaxation was significantly decreased in
CDH. These reports are not contrary to the present hypothesis that the PP fold mesenchymal cells greatly contribute to fusion between the right liver and the adrenal,
rather than fusion between the bilateral fold edges themselves. Difficulty with lung ascent may lead to CDH as a
result of defective lung development. It is well known
that an abnormal communication persisting between the
pleural and peritoneal cavities occurs more frequently on
the left. As anchoring of the liver to the dorsal structures
occurs on the right side, left-side separation along the coelomic mesothelium is likely to result in weakness there,
thus explaining the laterality of diaphragmatic hernia.
The process of switching from the ventrally located PP
fold to the retro-adrenal diaphragm in humans may differ
from that in mice because the mouse fetal adrenal seems
to be located far caudally to the lung bud (i.e., near the origin of the superior mesenteric artery; Babiuk et al., 2003).
Further studies of CDH-related genes will help not only to
clarify the process of diaphragm development but also to
obtain a comprehensive picture of how the topographical
anatomy of the thoracoabdominal viscera is regulated.
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Babiuk RP, Zhang W, Clugston R, Allan DW, Greer JJ. 2003.
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