1.

IMPLANTATION, EMBRYOLOGY,
& PLACENTAL DEVELOPMENT
Dr. Sia- Santocildes

Legend:
Williams

Lecture

INTRODUCTION

Hypothalamic-pituitary axis, ovaries, genital tract

Regulates the development of predictable, regular,

cyclical, and spontaneous ovulatory menstrual cycle.
25-32 days (25-35 Williams)

Cycle interval

Average of 28 days

June 27, 2013

LH theca cells secrete androgen (converted to

Estradiol).

Growth differentiation factor 9 (GDF9) and bone

morphogenic protein 15 (BMP-15)

Produced by oocytes

regulate proliferation and differentiation of granulose

cells as primary follicles grow.

Stabilize and expand cumulus oocyte complex (COC).

OVARIAN-ENDOMETRIAL CYCLE
I.

OVARIAN CYCLE

Fig. 1: Gonadotropin control of the ovarian and endometrial cycles.

The ovarian-endometrial cycle has been structured as a 28-day
cycle. The follicular phase (days 1 to 14) is characterized by rising
levels of estrogen, thickening of the endometrium, and selection of the
dominant ovulatory folicle. During the luteal phase (days 14 to
21), the corpus luteum (CL) produces estrogen and progesterone,
which prepare the endo-metrium for implantation. If implantation
occurs, the developing blastocysts will begin to produce human
chorionic gonadotropin (hCG) and rescue the corpus luteum, thus
maintaining progesterone production. FSH - follicle-stimulating
hormone; LH - luteinizing hormone.

A. Follicular Phase (Preovulatory Ovarian Phase)

2 million oocytes at birth

400,000 follicles at onset of puberty

Remaining follicles are depleted at a rate of 1,000/mo

until the age of 35.

Only 400 follicles are released during the female

reproductive life.

99.9% of follicles undergo atresia apoptosis

GnRH (hypothalamus) FSH (pituitary)

granulose cells secrete estrogen.

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Fig. 2: Two-cell-two-gonadotropin principle of ovarian steroid

hormone production
During the follicular phase (left panel), luteinizing hormone (LH)
controls theca cell production of androstenedione, which diffuses into
the adjacent granulosa cells and acts as precursor for estradiol
biosynthesis. The capacity for the granulosa cell to convert
androstenedione to estradiol is controlled by follicle stimulating
hormone (FSH). After ovulation (right panel), the corpus luteum forms
and both theca-lutein and granulosa-lutein cells respond to LH. The
theca-lutein cells continue to produce androstenedione, whereas
granulosa-lutein cells greatly increase their capacity to produce
progesterone and to convert androstenedione to estradiol. If pregnancy
occurs, the production of human chorionic gonadotropin (hCG) by the
placenta rescues the corpus luteum through the LH receptor. Lowdensity lipoproteins (LDL) are an important source of cholesterol for
steroidogenesis. cAMP- cyclic adenosine monophosphate.

Notes: During the follicular phase, estrogen levels rise in parallel to

the growth of dominant follicle and the increase of granulosa cells.
Granulosa cell is the exclusive site of the FSH. The increase in the
FSH during the late luteal phase of the previous cycle will stimulate
increase in FSH receptors and the ability of CP450 aromatase to
convert androstenediol to estrogen. The requirement for theca cell,s
which respond to the LH and granulose cells, which respond to the
FSH represent this theory.
FSH induces aromatase and expansion of the antrum of the growing
follicle. The follicle that is most responsive to the FSH is most likely
to be the first to produce estradiol and initiate the expression of LH
receptors. In the appearance of LH receptors, the preovulatory
granulosa cells secrete amounts of progesterone, which exerts positive
feedback on the estrogen on the pituitary to cause or augment LH
release. Granulosa cells also produce inhibin B which feedback on the
pituitary to inhibit release of the FSH.

Implantation, Embryology, & Placental Development Page 1 of 6

If theres a drop in FSH, theres failure of other follicles to reach

preovulatory status. During this time, the contralateral ovary is
relatively inactive.

Day 22-25 important feature is that glands exhibit

extensive coiling and luminal secretions become
visible.

B.

C.

Ovulation

Increase in estradiol LH surge

LH surge

10-12 hours before ovulation

Causes oocyte to be released from the follicle

Ruptured follicle becomes the corpus luteum, which

releases progesterone.

Day 23-28 predecidual cells appear.

Day 20-24 window of implantation

Note: The greater coiling of the spiral arteries marks angiogenesis.

Luteal Phase (Postovulatory Ovarian Phase)

Corpus luteum secretes progesterone for only about

11 days in the absence of the hCG.

17-estradiol

Secreted by granulosa cells of the dominant

follicle.

Most biologically potent naturally occurring

estrogen

Progesterone prepares the endometrium for

implantation.

Notes:
Corpus Luteum a transient endocrine organ within the
absence of pregnancy will rapidly regress 9-11 days after
ovulation.
In the process of luteolysis, there is a dramatic drop within the
circulating estradio and progesterone levels, which signals the
endometrium to initiate menstruation.
Estradiol has been proposed to act on the epithelial cells surface
to stimulate nitric oxide production leading to rapid vasoactive
properties

Fig. 3: The spiral arteries of human endometrium are modified during the
ovulatory cycle.

THE DECIDUA

II. ENDOMETRIAL CYCLE

A. Proliferative or Preovulatory Endometrial Phase

Epithelial glandular cells, stromal mesenchymal cells

and blood vessels of the endometrium replicate
cyclically.

Endometrium is regenerated during each ovarianendometrial cycle.

Functionalis layer superficial; shed and regenerated

from basalis layer (deeper layer).

5th day of cycle epithelial surface of the

endometrium has been restored and revascularization
is in progress.

This cycle is characterized by proliferation of vascular

endothelial, stromal, and glandular cells.

During early part of this phase:

Endometrium is thin (<2mm)

Glands are narrow, tubular structures that pursue
almost a straight and parallel course from the basalis
layer toward the surface of the endometrial cavity.
Mitotic activity in glandular epithelium persists until
day 16-17.

Late proliferative phase

B.

stromal cells surrounding the spiral arterioles begin to

enlarge, and stromal mitosis becomes apparent

Endometrium
thickens
from
both
glandular
hyperplasia and increased stromal ground substance

Secretory or Postovulatory Endometrial Phase

By day 17- glycogen accumulates in the basal portion

of the glandular epithelium, creating subnuclear
vacuoles and pseudostratification.
Day 18 vacuoles move to the apical portion of
the secretory nonciliated cells.

Day 19 cells begin to secrete glycoprotein and

mucopolysaccharide contents into the lumen.

Glandular cell mitosis ceases with secretory activity

due to rising progesterone levels, which antagonize the
mitotic effects of estrogen.
Estradiol is converted to the less active form estrone.

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A highly specialized, highly modified endometrium of

pregnancy
Decidualization the transformation of secretory
endometrium to decidua is dependent on estrogen,
progesterone, and the factors secreted by the implanting
blastocyst.

Fig. 4: Decidualized endometrium covers the early embryo. Three

portions of the deciduas (basalis, capsularis, and parietalis) also are
illustrated.

3 parts based on anatomical location

a. Decidua basalis the decidua directly beneath the
blastocyst implantation modified by trophoblast
invasion
b. Decidua capsularis the one that overlies the
enlarging blastocyst and initially separated it from the
uterine cavity
c. Decidua parietalis the decidua which lines the
remainder of the uterus

when the decidua capsularis and decidua

parietalis are joined termed together as
decidua vera

Implantation, Embryology, & Placental Development Page 2 of 6

2.

I.

DECIDUAL STRUCTURE

The decidua parietalis and basalis, like the secretory

endometrium, are composed of three layers
1. Zona compacta the surface or the compact zone
2. Zona spongiosa the middle portion, or spongy zone
with remnants of glands and numerous blood vessels
3. Zona basalis a basal zone

The zona compacta and zona spongiosa together form the

zona functionalis
The basal zone remains after delivery and gives rise to the
new endometrium

II. BLOOD SUPPLY

The blood supply to the decidua capsularis is lost as the

embryo-fetus grows consequence of implantation
Blood supply to the decidua parietalis persists via the
spiral arteries

These arteries retain a smooth muscle wall and

endothelium, thereby remaining responsive to
vasoactive agents that act on their smooth muscle or
endothelial cells
The spiral arterial system supplying the decidua basalis
directly beneath the implanting blastocyst is altered
remarkably

These spiral arteries and arterioles are invaded by

cytotrophoblasts

During this process, the walls of the vessels of the

basalis are destroyed and become unresponsive to
vasoactive agents.

III. DECIDUAL HISTOLOGY

The decidua contains numerous cell types, whose

composition varies with age of gestation

Zona compacta consists of large, closely packed,

epithelioid, polygonal, light-staining cells

with round nuclei

Zona spongiosa consists of large, distended glands

lined with cylindrical uterine epithelium early in
pregnancy; as pregnancy progresses, the epithelium
gradually becomes cuboidal or flattened; later in
pregnancy, the glandular elements largely disappear

Zona basalis contributes to the formation of the

basal plate of the placenta
Decidual natural killer cells (NK) present in the
decidua early in pregnancy

Likely play an important role in trophoblast invasion

and vasculogenesis
Nitabuch layer

A zone of fibrinoid degeneration in which invading

trophoblasts meet the decidua

Absence of this layer results to defective decidua

(as in placenta accrete)

IV. DECIDUAL PROLACTIN

3.
4.

Evidence suggests that the decidua is a source of prolactin

that is present in enormous amounts in amniotic fluid.
Prolactin preferentially enters amniotic fluid and little
enters maternal blood.
Prolactin levels:

In amniotic fluid extraordinarily high; may reach

10,000 ng/mL during 20-24 weeks

In fetal serum 350 ng/mL

In maternal serum 150-200 ng/mL

Roles of decidual prolactin:

Still unknown

Possible roles:
1. Transport of transmembrane solute and water,
and thus, maintenance of amniotic fluid volume

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Regulation of immunological functions during

pregnancy
o There are prolactin receptors in a number of
bone-marrow derived cells; prolactin may
stimulate T cells in an autocrine or paracrine
manner
Regulation of angiogenesis during implantation
Repression of genes detrimental to pregnancy
maintenance

IMPLANTATION, PLACENTAL
FORMATION AND FETAL MEMBRANE
DEVELOPMENT

During its brief intrauterine passage, the fetus is

dependent on the placenta for pulmonary, hepatic and
renal functions.
The placenta links the mother and the fetus by indirect
interaction with maternal blood that spurts into the
intervillous space from uteroplacental vessels.
Maternal blood bathes the outer syncytiotrophoblast to
allow exchange of gases and nutrients with fetal capillary
blood.
In this hemochorial placenta, fetal and maternal blood is
not normally mixed.

FERTILIZATION

The sperm penetrates the zona pellucida of a secondary

oocyte Meiosis II is triggered
Cortical granule reaction a propagated response of the
zona pellucida at the site of sperm entry and is a basis to
block polyspermy
Secondary oocyte Meiosis II Mature oocyte

Fig. 5: Zygote cleavage and formation of the blastocyst.

The period of the morula begins at the 12- to 16-cell stage and ends
when the blastocyst forms, which occurs when there are 50 to 60
blastomeres present. The zona pellucida has disappeared by the late
blastocyst stage (5 days). The polar bodies, shown in the 2-cell stage,
are small nonfunctional cells that soon degenerate.

IMPLANTATION

Implantation occurs 6th-7th day after fertilization

Postovulatory production of estrogen and progesterone by
corpus luteum Needed for development of receptive
epithelium.

20th-24th day of ovarian cycle.

Uterine receptivity only limited in this interval

After 24th day, less probability of adhesion due to
antiadhesive glycoproteins preventing receptor interactions.
At successful adhesion, blastocyst is at 100-250 cell-stage.
Paracrine interactions between trophoectoderm of the
blastocyst and endometrium regulates their adhesion and
adherence

Implantation, Embryology, & Placental Development Page 3 of 6

I.

PHASES OF IMPLANTATION

III. CHORIONIC VILLI

1.

Apposition

Initial adhesion of blastocyst to uterine wall

2.

most commonly occurs on the upper posterior

uterine wall
c.

Adhesions

Becomes distinguished at 12th day after fertilization into:

a. Cytotrophoblast core Primary Villi
b. Mesenchymal core Secondary Villi

integrins (mediates the adhesions of cells to the

extra cellular matrix proteins); most commonly are

3.

CAMs
Ex. V3 and 41
Marker of receptivity for blastocyst attachment
Abberant expression of V3 associated with infertility

Penetration and invasion of syncyciotrophoblast and

cytotrophoblast into the:
a. Endometrium
b.
inner 3rd of the myometrium
c.
uterine vasculature

Failure of angiogenesis hydatidiform mole

Villi are covered by outer layer of syncytium and inner
layer of cytotrophoblast

Anchoring Villi

Cytotrophoblast cell columns

Anchor to the decidua at basal plate

II. TROPHOBLAST IMPLANTATION

At 8 days after fertilization and implantation, trophoblast

differentiates into:
a. Syncytiotrophoblast: outer multinuclear
b. Cytotrophoblast: inner mononuclear

Germinal layer for the syncytium

Primary secretory component of placenta

Table 1. Cytotrophoblast vs. Syncitiotrophoblast.

CYTOTROPHOBLAST
Undergoes DNA synthesis
and mitosis
Well demarcated border
Single nucleus

SYNCITIOTROPHOBLAST
Amorphous
cytoplasm
without cell border
Nuclei multiple and diverse
in size and shape
Continuous syncytial lining

This configuration of the syncytiotrophoblast aids in transport

between them because control of transport is not dependent on
individual cells.

After implantation, trophoblast further differentiates

through 2 pathways:
1. Villous trophoblast chorionic villi

Chorionic villi primarily transport oxygen and

nutrients between the fetus and mother
2. Extravillous trophoblast

Migrates to:
a. Decidua
b. Myometrium
c.
Maternal vasculature

Classified as:
a. Interstitial trophoblast
o Invades decidua and myometrium to
form placental bed of giant cells
o Also, penetrates lumen of spiral arteries
b. Endovascular trophoblast

Hemochorial describes human placentation

Formerly called hemochorioendothelial, to take into
consideration the chotionic tissue separated from the fetal
blood by endothelial wall of the fetal capillaries.

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15th day maternal arterial blood enters intervillous

space
17th day fetal blood vessels functional and placental
circulation established
Fetal circulation is finished once embryonic vessels are
connected with chorionic vessels

Invasion: trophoblast

Angiogenesis Tertiary Villi

Increased contact between blastocyst and uterine epithelium.

mesenchymal cords derive from extraembryonic

mesoderm invade the solid trophoblast columns to
form secondary villi

Not invaded by fetal mesenchyme

The base of the intervillous space faces the maternal side and
consists of:
a. Cytotrphoblast from cell columns
b. Covering shell of syncytiotrophoblast
c.
Maternal deciua of the basal plate
The base of the chorionic plate forms the roof of the
intervillous space and consists of layers: external
trophoblasts and internal fibrous mesoderm
definitive chorionic plate formed 8-10 weeks by the
amniotic and primary chorionic plate mesenchyme
o
Formation accomplished by expansion of the amniotic
sac, which surrounds the connective stalk and allantois
to form umbilical cord

EMBRYONIC DEVELOPMENT AFTER

IMPLANTATION

10th day: blastocyst totally encase within the endometrium

9th day: Implantation of Blastocyst

Blastocyst wall at uterine cavity single layer

(blastocyst facing uterine wall)

Blastocyst wall at inner wall thicker wall, made

up of 2 zones:

Trophoblast

Inner cell mass: embryo-forming

7 days after fertilization: inner cell mass or embryonic
disc ectoderm mesoderm endoderm

Amniotic cavity: enclosing space between embryonic

disc and trophoblast

7 days after fertilization, the inner cell mass or

embryonic disc is differentiated into a thick plate of
primitive ectoderm and an underlying endoderm.
Some cells apper between the embryonic disc and the
trophoblast and enclose a space that will become the
amniotic fluid.

Isolated cells called mesenchyme enters blastocyst

cavity mesenchyme lines the cavity (mesenchyme
now called mesoderm; blastocyst cavity now called
chorionic vesicle; the layer made up of trophoblasts and
mesenchyme now called chorion)

Mesenchymal cells within amniotic cavity condense to form body

stalk umbilical cord

Implantation, Embryology, & Placental Development Page 4 of 6

PLACENTAL DEVELOPMENT

PLACENTAL GROWTH AND

MATURATION

I.

THE CHORION

Blastocyst and surrounding trophoblasts grows and expands into

the decidua expanding in 2 poles:
1. One outwards toward endometrial cavity
2. Opposite pole form placenta from villous trophoblasts and
anchoring cytotrophoblast

I.

PLACENTAL GROWTH

In first trimester, placental growth greater than fetus

17th postmenstrual week, plancental and fetal weights are

approximately equal
At term, placental weight is approximately 1/6 of fetal
weight with average characteristics of the ff:

diameter = 185mm.

thickness = 23 mm

volume = 497 mL

weight = 508 g.
10-38 lobes cotyledons

Composed of cytotrophoblast and fetal mesodermal

mesenchyme that survives in a relatively low oxygen
atmosphere
Chorion frondosum (leafy chorion)

the area of villi in contact with the decidua

basalis, fetal component of the placenta
Chorion laeve (smooth chorion)

contact with the decidual capsularis, a portion of

the chorion the becomes the avascular fetal
membrane that abuts the decidua parietalis
Its development is due to restricted blood supply of the
chorion facing the endometrial cavity
more tansparent than amnion, almost always <1mm in
thickness
sperated from amnion by the exocoelomic cavity until end of
3rd month
with the amnion, they are important sites of molecular
transfer and metabolic activity and they also constitute the
paracrine arm of the fetal-maternal communication system

Lobes are incompletely separated by grooves of variable

depth that overlie placental septa, which arise from folding
of basal plate
Number of lobes remain the same throughout gestation and
grow continuously but slows down at final weeks

II. PLACENTAL MATURATION

As villi branches Volume and prominence of

cytotrophoblasta decrease
As syncytium thins fetal vessels become prominent and
close to surface
Changes in the villous stroma:
1. In early pregnancy branching connective tissue
cells are separated by an abundant loose intercellular
matrix
2. In late pregnancy stroma is denser and cells more
spindly and more closely packed
3. Infiltration of Hofbauer cells
o fetal macrophages

As growth continues, uterine lumen is obliterated chorion

leave now contiguous with the entire maternal decidua parietalis
not occupied by placenta decidua capsularis merges with
parietalis as fetus grows capsularis lost due to pressure and
loss of blood supply are where parietalis and capsularis merge
in now called decidua vera

II. MATERNAL REGULATION OF TROPHOBLAST

INVASION AND VASCULAR GROWTH

Decidual Natural Killer Cells

(both promote
invasion of trophoblast cells to decidua toward spiral
IL-8 and INF inducible protein10
arteries)

FETAL CIRCULATION

VEGF, and placental growth factor (both promote

vascular growth in decidua)
Attract and promote invasion of trophoblast into the decidua
and promote vascular growth
Prevents from recognizing and destroying fetal cells as
foreign

accumulate in decidua in first half of pregnancy in direct

contact with trophoblasts

no cytotoxic activities yet (IMPORTANT: for preventing

recognition of fetal cells as foreign)

Deoxygenated venous-like fetal blood flows to plancenta through

2 umbilical arteries branches repeatedly in amnion and
dividing villi forms capillary networks in terminal divisions
high oxygen blood goes to fetus through umbilical vein

Chronic vessels (placental surface vessels)

Traverses the chorionic plate

Responsive to vasoactive agents

Chorionic arteries crossover chorionic veins but

cannot differentiate histologically

In 65% of placenta, chorionic arteries supply

cotyledons through fine network (disperse type
branching)

Remaining 35%, radiate to edges without narrowing

Both are end arteries that supply one cotyledon as

each branch turns downward to pierce chorionic
plate.

Truncal Artery

Perforating branch through chorionic plate

Supplies one cotyledon

III. UTROPLACENTAL VASCULATURE

2 waves of development:
1. Below 12 weeks post fertilization

Invasion and modification of the spiral artery up

to the border of the deciduas and myometrium
2. 12th 16th weeks post fertilization

Invasion of the intramyometrium segments of

spiral artery

These results to:

round with vesicular, eccentric nuclei and very

granular vacuolated cytoplasm
increases in number and maturation state through
pregnancy
capable of phagocytic, immunosuppressive,
cytokine-producing, and paracrine regulation of
trophoblast function

Narrow-lumen, muscular spiral arteries

dilated, low resistance uteroplacental vessels

Has pathogenesis associated with preeclampsia and fetal-growth

restriction

Increase in calibre of vessel and decrease in smooth muscle

as it penetrates chorionic plate

End diastolic flow within umbilical artery appears at 10

weeks AOG; no end diastolic flow before 10 weeks

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Outermost

relatively acellular zona spongiosa

contiguous with the second fetal membrane, chorion

laeve
lacks smooth muscles, nerves and lympathics; avascular
few fetal macrophages in the amnion

II. METABOLIC FUNCTIONS

Figure 6. Fetal Circulation.

2 umbilical artery (w/ deoxygenated blood) Placenta (containing chorionic
vessels and capillary network) Oxygenated blood
Umbilical vessels

MATERNAL CIRCULATION

1 month after conception, maternal blood enters the

intervillous space in fountain-like burst from spiral
arteries
Blood is propelled outside of the maternal vessels and
sweeps over and directly bathes the syncitiotrophoblast
Villous branching: Chorion frondosum Cotyledon:
single artery and vein

The chorion frondosum (or laevey chorion) the fetal

component of the placenta.
Maternal blood enters through the basal plate and is
driven high up toward the chorionic plate by arterial
pressure before laterally dispersing After bathing the
external microvillous surface of chorionic villi, maternal
blood drains back through venous orifices in the basal
plate and enters uterine veins
maternal blood traverses the placenta randomly without
preformed channels.
Spiral arteries: perpendicular to the uterine wall; Spiral
veins : parallel to the uterine wall - this arrangement aids
in the closure of veins during uterine contraction and
prevents entry of maternal blood from the intervillous
space

UMBILICAL CORD
Early in Pregnancy

Prominent yolk sac and umbilical vessicle into which it

develop

Dorsal surface grows faster than ventral surface

embryo bulges into the amniotic sac; dorsal part of the
yolk sac is incorporated into the body of the embryo to
form the gut

Allantois project into the base of the body stalk from the
caudal wall; later, form the anterior wall of the hindgut.

Yolk sac : smaller

Pedicle : longer
Middle and Third Month

Amnion fuse with chorion leave

Body Stalk umbilical cord or funis

At term

Cord : 2 arteries and 1 vein

Right umbilical vein disappears early during development

Arteries are smaller than vein

The most common vascular anomaly : absence of one

umbilical artery associated with fetal anomalies

Figure 7. Cross-section of umbilical

cord. The large umbilical vein carries
oxygenated blood to the fetus (above).
Below it, are the two smaller umbilical
arteries, carrying deoxygenated blood
from the fetus to the placenta.

AMNION

The inner most fetal membrane

Provide almost all of the tensile strenght of the fetal
membrane; at term, the amnion is a tough and tenacioius
but pliable membrane
Contiguous with amniotic fluid
Amniogenic cells precursors of amniotic epithelium
Identifiable by 7th or 8th day of embryonic development
Intially, a small minute vesicle small sac cover dorsal
surface of the embryo as it enlarge, engulfs embryo
prolapse into cavity adhere to chorion laeve
Near the end of the 1st trimester: apposition of the chorion
laeve and amnion causes obliteration of the
extraembryonic coelom.

I.

STRUCTURE OF AMNION

Inner

Bathed by amniotic fluid

Single layer of cuboidal epithelium from embryonal

ectoderm

Attached firmly to a distinct basement membrane

acellular compact layer composed primarily of
interstitial collagen
Outer

A row of fibroblast-like mesenchyme cells from

embryonic disk mesoderm

Contain amniotic fluid

Increase until 34 wks AOG

At term: 1,000ml
Involved in solute & water transport (maintain amniotic
fluid homeostasis)
Produce bioactive compounds

Extends from fetal umbilicus to the fetal surface of the

placenta or chorionic plate
Exterior: dull white, moist and covered by amnion
Diameter : 0.8 2cm
Length : 30-100 cm (average of 55 cm)
Abnormall short cord : < 30cm
Folding and tortousity vessels which are longer than cord
create surface nodulation false knot essentially varices
Extracellular matrix: Whartons jelly a specialized
connective tissue
Blood flow: two routes
1. Via ductus venosus empties into the inferior vena
cava
2. Numerous smaller openings into the hepatic
circulation
Blood exit: two umbilical arteries
Vessels contained in the cord spiral or twist.

Spiraling prevents cord crimping

-END-

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