Embryology of the Abdominal Wall and Associated Malformations-A Review

Abstract

In humans, the incidence of congenital defects of the intraembryonic celom and its associated structures has increased over recent decades. Surgical treatment of abdominal and diaphragmatic malformations resulting in congenital hernia requires deep knowledge of ventral body closure and the separation of the primary body cavities during embryogenesis. The correct development of both structures requires the coordinated and fine-tuned synergy of different anlagen, including a set of molecules governing those processes. They have mainly been investigated in a range of vertebrate species (e.g., mouse, birds, and fish), but studies of embryogenesis in humans are rather rare because samples are seldom available. Therefore, we have to deal with a large body of conflicting data concerning the formation of the abdominal wall and the etiology of diaphragmatic defects. This review summarizes the current state of knowledge and focuses on the histological and molecular events leading to the establishment of the abdominal and thoracic cavities in several vertebrate species. In chronological order, we start with the onset of gastrulation, continue with the establishment of the three-dimensional body shape, and end with the partition of body cavities. We also discuss well-known human etiologies.

Keywords: abdominal wall; congenital hernia; developmental cascade; embryology; human.

Figure 1

Schematic representation of the human organogenesis: Following fertilization the zygote transforms after cleavage and compaction into the blastocyst. At the end of the 2nd week the primitive streak appears on the surface of the embryo which is the first evidence of the beginning of gastrulation which ends with a trilaminar embryo. The notochord, a transient, rod-shaped structure induces neurulation and differentiation of the somites. Because of the rapid growth of the somites and the lateral plate mesoderm (LMP) the process of folding is initiated. The yolk sac is thereby incorporated into the embryonic body and the common body cavity is formed. The formation of the umbilical cord begins around week 3 with formation of the connecting stalk (CS). Approximately at week 7 the UC is fully established and is able to take over the metabolic functions. Physiologic herniation, due to the rapid growth of the intestine starts at week 6 and is terminated in the tenth week by its withdrawal into the embryonic body. If this does not take place, it comes to the formation of a omphalocele. If the amnion ruptures in the eighth to tenth week, gastroschisis results. The transverse septum (ST), which is located behind the base of the pericardial cavity separates the common body cavity incompletely since the pleuroperitoneal canals (PPC) on both sides are continuous between the two cavities. Due to the growth of the embryo, fusion of the pleuroperitoneal folds (PPF) occurs which leads to an occlusion of the canals. Morphogenetic defects of the PPF s subsequently prevent proper establishment of the costal muscles and its surrounding connective tissue with deficiencies in the diaphragmatic barrier. Differentiation of the inguinal canal closely is connected to differentiation of the gonads and their migration into the extracorporal scrotum together with the processus vaginalis, which is guided by the gubernaculum testis (GT). The IC acquires its adult morphology during the fetal period, due to the continuous growth of the abdominal muscles and wall, with the accompanying displacement of the inguinal rings. Failure in obliteration of the vaginal process will result in a patent processus vaginalis (PPV).

Figure 2

(A,B) Embryo GV-2 (6 somites). Stage 10 (4–12 somites; 2–3.5 mm; 22 days). Collection Orts LLorca (Complutense University of Madrid) Photos provided by Prof. J.F. Rodriguez-Vazquez. Oblique axial sections of the cephalic segment. (A) (4X) and (B) (10X). Staining: H-E. The trilaminar disc is located between the amniotic (ac) and yolk cavities (yc). In the ectoderm (ect) appears the neural groove (ng). The endoderm (end) is broken in segments. The mesoderm is divided into three segments: paraxial or somites (s), intermediate (im) and lateral (lm) mesoderm. The lateral mesoderm is split into the visceral/splanchnopleural (spl) and parietal/somatopleural (sol) layers. The notochord (n) appears as a cylindric structure with a cavity inside

Figure 3

(A,B) Embryo GV-2 (6 somites). Stage 10 (4–12 somites; 2–3.5 mm; 22 days). Collection Orts LLorca (Complutense University of Madrid) Photos provided by Prof. J.F. Rodriguez-Vazquez. Oblique axial sections of the future thoracic segment. (A) (4X) and (B) (10X). Staining: H-E. The trilaminar disc is located between the amniotic (ac) and yolk cavities (yc). In the ectoderm (ect) appears the neural tube (nt). The endoderm (end) is broken in segments. The mesoderm is divided into three segments: paraxial or somites (s), intermediate (im) and lateral (lm) mesoderm. The lateral mesoderm is split into the visceral/splacnopleural (spl) and parietal/somatopleural (sol) layers. The notochord (n) appears as a double structure due to the obliquity of the section.

Figure 4

Embryo GV-5 (4 mm). Stage 11 (13–20 somites; 2.5mm-4.5 mm; 24 days). Collection Orts LLorca (Complutense University of Madrid). Photo provided by Prof. J.F. Rodriguez-Vazquez. Axial section of the thoracic segment (4X). Staining. H-E. The section shows the pericardic cavity (pc) surrounding the ventriculus (v) and bulbus (b) cordis. Dorsal of this is the transverse septum (ts). The liver diverticula emerging from the anterior gut (ag) which are growing stringy into the the transverse septum (arrows) are visible. The anterior gut is surrounded by the umbilical (uv) and vitelline veins (vv). pleuroperitoneal cavity (ppc), amniotic cavity (ac), secondary yolk cavity (yc), duplicate aorta (ao), neural tube (nt) and the notochord (n)

Figure 5

(A–C) Embryo A (13 mm). Stage 17 (41 days). Collection Javier Puerta (Complutense University of Madrid). Axial sections of the upper thoracic (A), lower toracic (B), upper abdominal level (C) segments (2X). Staining: H-E. In this sections it is possible to see the course of the phrenic nerves in the pericardial membranes until reach the diaphragm (arrows). Moreover, it is possible to see the aorta (ao) as wells as the esophagus accompanied by the vagus nerves (X). lungs (lu) and heart (h)

Figure 6

(A,B) Embryo BI-8.5 (8.5 mm). Stage 15 (33 days). Collection Jvier Puerta (Complutense University of Madrid). Axial sections of the upper thoracic (A) and lower toracic (B) segments (2X). Staining: H-E. This sections shows the liver cords (li) growing into the transverse septum (ts) with the consequence increase of the liver size The diaphragm (arrows) is located between the pericardial cavity surrounding the heart and the primitive liver as a dense mesenchymal condensation. The pleuroperitoneal cavity still remains continuous. anterior gut (ag), stomach (s), bulbus (b) and ventriculus (V) cordis, umbilical vein (uv), right primary bronchi (lu), mesonephros (m).

Figure 7

(A–C) Embryo A (13 mm). Stage 17 (41 days). Collection Javier Puerta (Complutense University of Madrid). Axial sections of the upper thoracic (A), lower thoracic (B), upper abdominal (C) segments (all 2X). Staining: H-E. liver (li), sternal, costal, lumbar (arrows) and vertebral portions of the diaphragm (*). The pleuroperitoneal cavity still remains continuous. heart (h) aorta (ao), right bronchi (lu).

Figure 8

(A,B) Embryo DD-10 (10 mm). Stage 16 (37 days). Collection Javier Puerta (Complutense University of Madrid). Axial sections of the thoracic (A) and upper abdominal (B) segments (2X). Staining: H-E. These sections show the liver cords (li) growing into the transverse septum (ts) with the consequence increase of the liver size. The diaphragm (arrows) is located between the pericardial cavity surrounding the heart and the primitive liver as a dense mesenchymal condensation. The pleuroperitoneal cavity continues to communicate. anterior gut (ag), stomach (s), bulbus (b) and ventriculus (V) cordis, umbilical vein (uv), right bronchi (lu), mesonephros (m).

Figure 9

Embryo HA-24 (24 mm). Stage 22 (54 days). Collection Javier Puerta (Complutense University of Madrid). Sagittal section of the trunk (1X). Staining: Picro. The descensus of the diaphragm and its typical dome shape, with the anterior sternal and posterior vertebral attachments is shown (arrows). The hole in the phrenic center is visible with the inferior vena cava (ivc) and behind these structures the descensus of the esophagus (oe) and aorta (ao) for passing through their corresponding hiatus. Clavicle (cl), mandible (ma), spine (sp), duodenum (d), pancreas (p), gonad (g), liver (li), heart (h) lung (lu), trachea (t) and physiological hernia (ph)

Figure 10

(A,B) hernia of the intestine into the left pleural cavity (Bodaleck) of a neonate. After removing the intestinal contents the diaphragm (arrows) the permanent defect of the pleuroperitoneal membrane (arrowheads) is visible. The left lung (lu) has been displaced leftwards.

Figure 11

(A) Embryo ES20 (20), (Stage 20, 51 days), axial section (1X), Staining: H-EF. (B) Embryo VD-34 (34 mm), (57 days), axial section (1X), Staining: Bielschowsky, Collection Javier Puerta (Complutense University of Madrid). Physiological hernia and its narrowing during the embryonic period (arrows). In these sections, you can see the loops of intestine in the umbilicus and the narrowing umbilical orifice. gut (g), stomach (s), liver (li), umbilical vein (uv), umbilical artery (ua), gonad (go), pancreas (p), vitelline vein (vv)

Figure 12

Fetus F88 (88 mm), (12th weeks). Collection Javier Puerta (Complutense University of Madrid). Axial section of the trunk (1X). Staining: Azan.In this section the umbilicus (umb) and the anterolateral abdominal muscles: rectus abdominis (ar), external oblique (eo), internal oblique (io) and transversus (t) abdominal muscles are visible. M. psoas (ps) and M. quadratus lumbarum (ql). common iliac arteries (cia), ureter (u), intestinal loops (g) and the contents of the umbilicus, the umbilical arteries (ua) and vein (uv)

Figure 13

Fetus F25 (60 mm), (10th weeks). Collection Javier Puerta (Complutense University of Madrid). Sagittal section of lower third of the abdominal cavity (2X). Staining: Azan. The gubernaculum testis (gt) inside the inguinal canal and surrounded by the vaginal process (vp) is visible. The testicle (t) is located dorsally of the internal ring of the inguinal canal. external oblique (eo) muscle, conjoint tendon (ct).

Figure 14

Dissection of the lower abdominal wall and scrotum in a male neonate (BOU; 30.2 cm; 28–32 weeks) with the testicle (t) inside the peritoneal cavity located dorsally of the internal inguinal ring and the Gubernaculum testis (gt) as an amorph substance; sc, scrotum; intestine (g), p, penis; umb, umbilicus.

Figure 15

Fetus F14 (48 mm). (9th weeks). Collection Javier Puerta (Complutense University of Madrid). Sagittal sections (A and B) of the trunk (1X). Staining: Azan. The inguinal canal (ic), inguinal ligament (il), the external oblique muscle (eo) and the transverse (t) and internal oblique muscles (io) are visible. Inside the inguinal canal the gubernaculum testis is located which has become in this case of a female specimen the round ligament (rl) connected with the uterus (u). ovary (o), Fallopian tube (Ft), ureter (ur), external iliac artery (eia), pubis bone (pu), intestinal loops (g) in the peritoneal cavity.