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Embryogenesis

Last updated: August 10, 2020

Summary

Embryogenesis is the process of embryonic development occurring in the first eight weeks after fertilization. After implantation of the blastocyst in the endometrium, the embryo consists of the embryoblast and the trophoblast. While the embryoblast further develops into different structures of the body, the trophoblast is mainly involved in the development of the placenta. The amniotic cavity, yolk sac, extraembryonic mesoderm, and the chorionic cavity develop during the second week. In weeks 3 and 4, the bilaminar disc differentiates into a trilaminar embryonic disc through the process of gastrulation. A number of structures develop from the three germ layers. The nervous system also develops during weeks 3 and 4 through the process of neurulation. Weeks 5–8 are mainly characterized by organogenesis and continued differentiation of embryonic tissue.

Overview

First week of embryonic development (days 1–7)

See stages of pregnancy.

Overview of the 1st week of pregnancy and embryogenesis

Second week of embryonic development (days 8–14)

Embryoblast → bilaminar disc (epiblast and hypoblast)
- Epiblast → amniotic cavity
- Hypoblast → yolk sac, lining of chorionic cavity
Trophoblast → chorionic cavity (lined by extraembryonic mesoderm) → cytotrophoblast and syncytiotrophoblast → fetal component of the placenta

Day 8 of embryogenesis: formation of the amniotic cavity Day 9 of embryogenesis: formation of the yolk sac Day 12 of embryogenesis: formation of the extraembyonic mesoderm Day 13 of embryogenesis: formation of the chorionic cavity Second week of embryogenesis (overview)

3^rd and 4^th week of embryonic development (days 15–28)

Gastrulation: Epiblast cells → primitive streak → trilaminar disc (endoderm, mesoderm, ectoderm)
Notogenesis: axial mesoderm → notochord → induces development of neural plate from ectoderm
Neurulation: ectoderm → neural plate → neural tube with neural pores, neural crest
Branchial apparatus → pharyngeal arches, pharyngeal pouches, pharyngeal grooves
Aortic arches
Morphogenesis
Differentiation of the germinal disc
Primitive circulation with a tubular heart and initial intraembryonic blood vessels
Development of upper and lower limb buds

The embryo is extremely susceptible to teratogens from week 3 to week 8, when the process of organogenesis occurs. Endodermal developments

Fifth to eighth week of embryonic development (days 29–56)

Weeks 5–8 of embryogenesis mainly involves organogenesis and continued differentiation of the embryo. Organogenesis is complete by the end of week 8. In the subsequent fetal period, the fetus grows and develops.

	Characteristics
Week 5	Rapid head growth through development of the brain and facial structures The mesonephros, which is formed between weeks 3 and 5, bulges in the urogenital ridge. Development and differentiation of additional pharyngeal arches
Week 6	Digital ray development Auricular hillock development, which later becomes the auricle Eye is clearly recognizable through retinal pigment development Back starts to straighten Formation of a physiological umbilical hernia Fetal heart beats are visible on transvaginal ultrasound.
Week 7	The proximal bones of the upper limbs start to ossify.
Week 8	Recognizable human form Fingers are initially separated from one another by skin flaps, followed by complete separation. The proximal bones of the lower limbs start to ossify. Genitals have sex-specific characteristics; however, these are not yet sufficient to determine sex on ultrasound. Fetal movements begin.

Embryoblast and trophoblast development

Embryoblast

In the 2^nd week of embryonic development (days 8–14), the embryoblast differentiates into two layers (epiblast and hypoblast), termed the bilaminar disc. After formation of the amniotic cavity and yolk sac, the bilaminar disc is sandwiched between them.

Embryoblast → bilaminar disc
- Epiblast: columnar cells adjacent to amnioblasts → form the amniotic cavity → forms the embryo (begins the 3^rd week of embryonic development)
- Hypoblast: cuboidal cells adjacent to the blastocyst cavity (blastocoel); : forms yolk sac, lining of chorionic cavity
- Fusion of epiblast and hypoblast → prechordal plate → mouth

Development of the yolk sac and amniotic cavity

All three germ layers (ectoderm, mesoderm, and endoderm), as well as the amniotic cavity and therefore the entire embryonic tissue, arise from the epiblast. The extraembryonic mesoderm and the yolk sac are derived from the hypoblast.

The bilaminar disc forms the dividing layer between the yolk sac and amniotic cavity.

Trophoblast

The trophoblast is the layer of cells that surrounds the blastocyst. During week 2, the trophoblast divides into two layers, the cytotrophoblast and the syncytiotrophoblast. They form the embryonic component of the placenta.

Cytotrophoblast: the inner layer; mitotically active
- Function: cells migrate outward and fuse to become the syncytiotrophoblast
Syncytiotrophoblast: the outer layer; mitotically inactive
- Function: invades the endometrium to create lacunae (spaces that fill with maternal blood)
  - Secretes beta-hCG to maintain the corpus luteum and the decidua (starts when implantation of the blastocyst occurs)
  - Invades the endometrium to create lacunae (spaces that fill with maternal blood)
    - Proteolytic enzymes secreted by the syncytiotrophoblast break down the extracellular matrix
    - Formation of vacuoles within the syncytiotrophoblast, fusion of vacuoles to form lacunae (lacunar stage)
    - Invasion of syncytiotrophoblast into maternal capillaries (sinusoids)
    - Maternal sinusoids and lacunae fuse; maternal blood flows through the trophoblast → uteroplacental circulation
Formation of the chorionic cavity
- Starting point: The amniotic cavity and primary yolk sac are surrounded by trophoblast cells.
- Sequence of events
  - The trophoblast grows significantly faster than the surrounding structures → a gap forms between it and the amniotic cavity.
  - The gap is lined by the extraembryonic mesoderm.
  - Renewed gap formation in the extraembryonic mesoderm results in the formation of a new cavity
  - The extraembryonic mesoderm splits into two layers (somatopleuric and splanchnopleuric mesoderm) but remains attached at a connecting stalk
    - Somatopleuric (parietal) mesoderm: lines the trophoblast
    - Splanchnopleuric (visceral) mesoderm: surrounds the amniotic cavity and yolk sac with an intermediate germinal disc
    - Extraembryonic coelom (chorionic cavity)
      - Cavity that is formed between the somatopleuric and splanchnopleuric layers → precursor of the gestational sac
      - Lined by the chorion (outermost cell layer surrounding the embryo)
    - Connecting stalk
      - A derivative of extraembryonic mesoderm that connects the amniotic cavity and primitive yolk sac to the chorion
      - Precursor of the umbilical cord

The extraembryonic coelom is also called the chorionic cavity, which is lined by the chorion.

References:^[1]

Gastrulation

Gastrulation is the formation of the trilaminar embryonic disc or gastrula through the migration of epiblast cells. Epiblast cells migrate through the primitive streak between the epiblast and hypoblast layers and form an intermediate cell layer called the intraembryonic mesoderm. The hypoblast is replaced by epiblast cells, from which the endoderm arises. The original epiblast becomes the ectoderm.

Origin: primitive streak, an elongated accumulation of epiblasts
Result: formation of the trilaminar embryonic disc (mesoderm, endoderm, and ectoderm)
Process: occurs weeks 3–4
- Mesoderm development (intraembryonic mesoderm)
  - Epiblast cells detach from the cellular complex below the primitive streak → formation of the primitive pit
  - Mesoderm cells migrate through primitive pit
  - Proliferation of cells on both sides of the primitive pit and formation of the mesoderm, a new layer between the epiblast and the hypoblast
- Endoderm development
  - Epiblast cells migrate from the primitive streak and the primitive node to the hypoblast layer.
  - Hypoblast cells are invaded by epiblast cells and form an additional germ layer called the endoderm.
- Ectoderm development: differentiation of remaining epiblast cells into ectoderm after migration of cells for endoderm, mesoderm, and notochord

All embryonic tissue originates from the epiblast!

Gastrulation Derivatives of the ectoderm

Notogenesis

Definition: : development of the notochord, a rodlike structure between the ectoderm and endoderm that is essential for the development of the nervous system and primitive skeletal structures
Location: the notochord migrates along the primitive streak (the future craniocaudal axis), and ends at the prechordal plate. It is part of the axial mesoderm
Process: occurs weeks 3–4 (at the same time as development of the trilaminar embryonic disc)
- Epiblast cells migrate from the primitive nodes and extend cranially to form the notochordal process.
- Notochordal process margins converge until they merge into the rod-shaped notochord at the end of week 4
Derivatives
- The notochord degenerates during the course of embryogenesis.
- The nuclei pulposi of the intervertebral discs are remnants of the notochord.

Neurulation

Neurulation is the formation of the neural tube and neural crests, which are the precursors to the central and peripheral nervous systems. During this process, the surface ectoderm is also formed, which gives rise to the epidermis.

Definition: formation of the neural tube and neural crests via neural plate folding
Process:
- The notochord secretes signaling molecules that trigger differentiation of the medial ectoderm (located directly above the notochord) into neural cells.
- This region is termed the neural plate.
Sequence
- The central area of the neural plate decreases (invagination) and becomes the neural groove.
- The neural folds are found on both longitudinal sides of the neural groove.
- The neural folds converge (week 3) and convert the neural groove into the neural tube.
  - The dorsal-most part of the neural tube forms the specialized neural crest.
- The neural tube communicates with the amniotic cavity through cranial and caudal openings (neuropore).
  - Anterior neuropore: closes on ∼ days 24–25
  - Posterior neuropore: closes on ∼ days 26–27
- Fusion of the opposite sides of the neural folds results in the formation of the surface ectoderm.
- Neural fold fusion leads to several cells dissociating from the epithelial cluster, which deposit between the neural tube and surface ectoderm as the neural crest cells.
Derivatives
- Neural tube: forms the central nervous system (brain and spinal cord) and retina
- Neural crest: differentiates into different cell types, including neurons, dorsal root ganglia, and glia of the peripheral nervous system
- Surface ectoderm: forms the epidermis

The entire nervous system develops from the ectoderm!

Neural tube defects are one of the most common CNS malformations and develop as a result of incomplete closure of the neural tube (e.g., spina bifida, anencephaly).

Neurulation Neurulation (∼ day 18) Embryogenesis of the spinal cord, vertebral column, and intervertebral disc Spina bifida cystica

Branchial apparatus

Definition: An embryological structure with five paired arches composed of mesodermal and neural crest cells bound externally by an ectodermal cleft and internally by an endodermal pouch, which differentiate into various head and neck structures. The branchial apparatus is externally visible below the developing brain of a 4-week-old embryo. The fifth arch regresses in utero and does not contribute to the development of any head and neck structures.

Pharyngeal arch: the central mesenchymal core, which contains a nerve, an artery, and cartilage
Pharyngeal pouch: endodermal origin
Pharyngeal groove: ectodermal origin

Pharyngeal arches overview

Pharyngeal arches

Pharyngeal arch derivatives
Pharyngeal arch	Nerve	Artery	Muscle	Skeletal structure
First pharyngeal arch (mandibular arch)	CN V₃	Maxillary artery	Muscles of mastication Mylohyoid muscle Digastric muscle, anterior belly Tensor tympani muscle Tensor veli palatini muscle	Mandibular prominence Meckel cartilage: malleus, incus Mandible Maxillary prominence Zygomatic bone Palatine bone Squamous temporal bone Vomer
Second pharyngeal arch (hyoid arch)	CN VII	Obliterates completely	Muscles of facial expression (see development of the face) Digastric muscle, posterior belly Stylohyoid muscle Stapedius muscle	Stapes Styloid process Stylohyoid ligament Hyoid bones Lesser horn and body
Third pharyngeal arch	CN IX	Common carotid artery Internal carotid artery External carotid artery	Stylopharyngeus muscle	Hyoid bones: greater horn and body
Fourth pharyngeal arch	CN X Superior laryngeal nerve	Left: aortic arch Right: subclavian artery	Middle and inferior pharyngeal constrictor muscles Cricothyroid muscle Palatopharyngeus muscle	Upper part of thyroid cartilage
Sixth pharyngeal arch	CN X Recurrent laryngeal nerve	Left: ductus arteriosus Truncus pulmonalis, left pulmonary artery Right pulmonary artery	Internal larynx muscles	Lower part of thyroid cartilage Arytenoid cartilage Corniculate cartilage Cuneiform cartilage

Pharyngeal arch derivatives Meckel cartilage

Pharyngeal pouch

Derivatives
- First: eustachian tube, tympanic cavity
- Second: palatine tonsil, supratonsillar fossa
- Third
  - Dorsal wings: inferior parathyroid glands
  - Ventral wings: thymus
- Fourth
  - Dorsal wings: superior parathyroid glands
  - Ventral wings: ultimobranchial body, parafollicular cells (C cells) of the thyroid

The inferior parathyroid glands arise cranially (3^rd pouch) but end up caudally (lower poles of the thyroid gland). The superior parathyroid glands arise caudally (4^th pouch) but end up cranially (superior poles of the thyroid gland).

Endodermal development

Pharyngeal grooves

Derivatives
- The first pharyngeal groove develops into the external auditory meatus, the auditory canal, and the external aspect of the tympanic membrane.
- The second to fourth pharyngeal grooves are obliterated in-utero by the rapid growth of the second pharyngeal arch, and they do not differentiate into any of the head and neck structures.
Cervical sinus
- The second pharyngeal arch develops faster than the others → overlap and merge with the second and third arches → grooves lose their connection with the amnion → cervical sinus is formed.
- The cervical sinus is obliterated during later development.
- Failure of the cervical sinus to obliterate completely results in branchial cleft sinus, which can lead to lateral cervical fistula.

A lateral cervical fistula is prone to infection and is a clear indication for operative treatment!

Aortic arches

The aortic arches are blood vessels that run in between the pharyngeal pouches and form the major head and neck arteries. The arches develop in craniocaudal order, with the first two arches obliterating early and the fifth either never developing or also obliterating without giving rise to a vessel.

Aortic arches	Derivatives
First	Maxillary artery: remnant of obliterated first arch
Second	Most parts of the second aortic arch obliterate early Hyoid artery: remnant of the largely obliterated second arch Stapedial artery: transient branch of the hyoid artery (typically regresses around week 10 of development)
Third	Common carotid Proximal internal carotid
Fourth	Right: proximal right subclavian artery Left: aortic arch (from left common carotid to left subclavian)
Sixth	Right: right pulmonary artery Left: left pulmonary artery, ductus arteriosus

1^st is maximal (maxillary artery); Second for Stapedial; C is the 3^rd letter of the alphabet (Common Carotid, proximal internal Carotid); 4^th arch and 4 limbs (systemic arch).

Aortic arch derivatives

Morphogenesis

Morphogenesis is the process by which the shape of an organism is generated. The embryo undergoes folding, resulting in transformation of the flat, embryonic disc into an embryo that approaches the human form during the course of the pregnancy. During the folding processes, the abdominal cavity, the abdominal wall, and the gut tube are formed. At the cranial and caudal embryonic poles, there is an area devoid of the mesoderm where the endoderm and ectoderm come into direct contact with one another, called the buccopharyngeal or cloacal membrane. The mouth and anus will later form in these areas.

Body axis determination

Dorsoventral body axis: formed as the bilaminar disc develops
- Dorsal body axis: epiblast
- Ventral body axis: hypoblast
Craniocaudal body axis: formed by the extension of the primitive streak
- Cranial pole: primitive nodes
Right-left differentiation: The positioning of unpaired chest and abdominal organs is determined by asymmetric expression of signaling molecules in the lateral plate mesoderm.

Situs inversus is a very rare congenital condition in which the chest and abdominal organs are reversed or mirrored. It is usually considered a benign condition, but can also present as part of a syndrome, e.g., Kartagener syndrome.

Situs inversus

Craniocaudal folding

Process: The cranial and caudal embryonic poles curl, resulting in curving of the embryonic disc.
Result:
- The embryo develops a C form.
  - Caudal end: tail fold
  - Cranial end: head fold
- Constriction of the yolk sac

Lateral folding

Process
- Ventral outgrowth of the lateral margins of the embryonic disc
- The ectoderm and the overlying lateral plate mesoderm on both sides converge.
- Adhesion of both sides results in the formation of a lateral and anterior body wall as well as a cavity, the intraembryonic coelom
- The endoderm and the overlying lateral plate mesoderm on both sides converge → gut tube formation
Result
- Intraembryonic coelom
- Gut tube
  - Anterior end of the foregut
  - Foregut
  - Midgut
  - Hindgut
- Further constriction of the yolk sac

Craniocaudal and lateral folding (embryogenesis)

The midgut stays connected to yolk sac remnants via the vitelline duct (omphalomesenteric duct). This duct is obliterated during the course of embryogenesis. Persistence of this duct most commonly results in Meckel diverticulum but could also cause retroumbilical cysts and fistulae.

Buccopharyngeal and cloacal membrane formation

Process
- Buccopharyngeal membrane: region without mesoderm at the cranial embryonic pole
  - Stomodeum: formation as a result of deep depression by the buccopharyngeal membrane due to expansion of the brain
  - The buccopharyngeal membrane ruptures shortly after folding → development of a link between the stomodeum (and therefore also the amniotic cavity) and the gut tube
- Cloacal membrane: region without mesoderm at the caudal embryonic pole
  - Proctodeum formation as a result of inward folding of the ectoderm
  - The cloacal membrane tears significantly later than the buccopharyngeal membrane → a link develops between the amniotic cavity and urogenital tract/anal canal
Results
- Formation of future body orifices
- The embryo is connected to its external environment (e.g., amniotic fluid) via the body orifices.

Abnormalities of morphogenesis

Process	Definition	Characteristics	Example
Agenesis	The organ is not present.	Primordial tissue from which the organ is derived is absent.	Agenesis of the corpus callosum Renal agenesis Müllerian agenesis
Aplasia	The organ is not present.	Primordial tissue from which the organ is derived is present.	Aplasia cutis congenita Thymic aplasia
Hypoplasia	Underdevelopment of an organ	Primordial tissue from which the organ is derived is present.	Hypoplastic right heart syndrome
Disruption	Breakdown of a previously normal structure or tissue		Amniotic band syndrome Entrapment of fetal parts in fibrous amniotic bands Clinical features Constriction rings or bands Autoamputation of digits or limbs Syndactyly Abdominal wall defects, visceral protrusions Craniofacial anomalies
Deformation	Interruption of the normal development of an organ due to an extrinsic force (e.g., in case of multiple gestations or big leiomyomas)	Occurs after week 8	Congenital talipes equinovarus Congenital torticollis
Malformation	Interruption of the normal development of an organ due to an intrinsic process	Occurs between week 3 and week 8	Arnold-Chiari malformation Arteriovenous malformation (an abnormal connection between arteries and veins bypassing capillaries which develops due to disrupted angiogenesis)
Sequence	A single event that causes multiple abnormalities		Pierre Robin sequence Potter sequence
Syndrome	A set of clinical features that consistently occur together	Commonly caused by genetic mutations (e.g., trisomy 21)	Down syndrome Patau syndrome Edward syndrome

Hand affected by amniotic band syndrome

References:^[2]^[3]^[4]

Differentiation of the germinal disc

Differentiation of the mesoderm

Axial mesoderm

Location: central region of the mesoderm
Components: notochord and prechordal mesoderm

Paraxial mesoderm

Location: tube-shaped area of the mesoderm surrounding the notochord
Components: somites
Process:
- The paraxial mesoderm becomes divided into segmented round cell clusters (somites) along the neural tube (week 4)
- Up to the beginning of week 5, an initial 42–44 somite pairs are formed in a craniocaudal direction.
- Degeneration of several somite pairs, so that 35–37 somite pairs remain
- As primitive segments, somites determine body segmentation
  - Somite segments
    - Sclerotome: medial migration of cells toward the notochord and fusion of both sclerotomes of a somite pair
    - Dermomyotome
      - Dermatome: migration toward the surface ectoderm
      - Myotome: subdivision into the dorsal epimere and ventral hypomere skeletal muscles in the lateral and anterior regions of the thorax and abdomen

Somites development

Intermediate mesoderm

Location: lateral to the paraxial mesoderm
Components: urogenital fold, consisting of the nephrogenic ridge and genital ridge

Lateral plate mesoderm

Location: lateral to the intermediate mesoderm
Sequence of events
- In the second week of development, small folds develop in lateral aspect of the mesoderm.
- These folds split horizontally to form two components.
  - Somatic (parietal) mesoderm: the dorsal layer that underlies the ectoderm and differentiates into the lining of the pleural, pericardial, and peritoneal cavities.
  - Splanchnic (visceral) mesoderm: the ventral layer that overlies the endoderm and differentiates into the visceral lining of internal organs.
- The space between these components is called the coelom
- The two coeloms from either side fuse at the end of the lateral folding of the embryo to form one large cavity, the intraembryonic coelom, which will differentiate into the thoracic and abdominal cavities (see “morphogenesis” above).

Mesenchyme ≠ mesoderm: The mesoderm is one of the three germinal layers that differentiates into different tissues. The mesenchyme is embryonic connective tissue that develops from the mesoderm and other germ layers.

Embryonic mesoderm

Fate mapping

A fate map is used to determine the origin of a cell lineage, e.g., a germ layer. The following table provides an overview of the various tissue types and structures that arise from the three germ layers.

Germ layer structure			Differentiated tissue/organs
Ectoderm	Neuroectoderm (neural tube)		Central nervous system (except the anterior pituitary) Retina Pineal gland Posterior pituitary (neurohypophysis) Astrocytes Oligodendrocytes
	Neural crest		Nervous tissue Neurons and glia of the peripheral nervous system, dorsal root ganglion , autonomic ganglion, Schwann cells, satellite glial cells Enteric nervous system Mesenchyme cells of the cranial mesectoderm Dermis and subcutaneous tissue in the head region Bones, cartilage, and connective tissue of the head region Arachnoid mater and pia mater Odontoblasts (dentin) and dental cement Other cell types Chromaffin cells of the adrenal medulla Skin melanocytes Carotid body Cardiac septum in the outflow tract Cardiac tissue Endocardial cushions Aortopulmonary septum
	Surface ectodermal placodes		Olfactory epithelium Inner ear Lens Cranial nerve ganglia (partial)
	Surface ectoderm		Epithelium Oral cavity, nasal cavity, paranasal sinuses, lacrimal ducts, ear canal Epidermis and skin appendages Hair, nails, glands including mammary glands Other cell types Ameloblasts (enamel organ) of the teeth Anterior pituitary Parotid gland Inner ear sensory organs
Mesoderm (intraembryonic mesoderm)	Axial	Prechordal	Bones that make up the base of the skull (partially) Extraocular muscles
	Axial	Notochord	Nucleus pulposus of the intervertebral discs
	Paraxial	Sclerotome	Vertebral body and vertebra Annulus fibrosus of the intervertebral discs Ribs
		Dermatome	Spinal meninges Dermis and cutis of the back and partially the head
		Myotome	Skeletal muscles Neck (hypomere) Lateral and ventral trunk wall (hypomere) Intrinsic back muscles (epimere) Limbs (hypomere)
	Intermediate		Kidneys (pronephros, mesonephros, metanephros) Gonads Renal and genital excretory ducts
	Lateral plate mesoderm	Splanchnic (splanchnopleuric) mesoderm	Cardiovascular system Heart Blood vessels Stem cells of erythroid, lymphoid, and myeloid origin Lymph nodes and vessels Other cell types Adrenal cortex Spleen Visceral layers of the pericardium, pleura, and peritoneum Connective tissue and smooth muscle of the intestinal wall
	Lateral plate mesoderm	Somatic (somatopleuric) mesoderm	Connective tissue of the anterior and lateral trunk wall Parietal layers of the pericardium, pleura, and peritoneum Smooth muscle of the viscera Sternum Limbs (except the muscles)
Endoderm			Epithelium Thyroid, parathyroid Pharynx Eustachian tube Tonsils Thymus Epithelium and glands Esophagus and gastrointestinal tract (except the parotid gland) Liver, gallbladder, pancreas Respiratory tract Bladder, prostate, urethra, and distal vagina Parafollicular cells (C cells) in the thyroid

Primitive gut (4th week of development) Endodermal development Neurulation (∼ day 18) Mesoderm derivatives

References:^[5]

References

Sadler TW. Langman's Medical Embryology. Lippincott Williams & Wilkins ; 2011
Le T, Bhushan V, Sochat M, Chavda Y. First Aid for the USMLE Step 1 2017. McGraw-Hill Education ; 2017
Le T, Bhushan V,‎ Sochat M, Chavda Y, Zureick A. First Aid for the USMLE Step 1 2018. McGraw-Hill Medical ; 2017
Kadian YS, Verma A, Rattan KN, Kajal P. Vitellointestinal duct anomalies in infancy. J Neonatal Surg. 2016; 5 (3): p.30. doi: 10.21699/jns.v5i3.351 . | Open in Read by QxMD
Coelomic Cavity Development. https://embryology.med.unsw.edu.au/embryology/index.php/Coelomic_Cavity_Development. Updated: April 30, 2018. Accessed: June 28, 2018.