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Chapter 30 ■ The First Trimester 1077
A
B
FIGURE 30-4. Formation of secondary yolk sac. A, Approximately 26 days: formation of cavities within extraembryonic
mesoderm. These cavities will enlarge to form extraembryonic coelom. B, About 27 days, and C, 28 days: formation of secondary yolk
sac with extrusion of primary yolk sac. Extraembryonic coelom will become chorionic cavity. (From Moore KL, Persaud TVN, editors. The
developing human: clinically oriented embryology. 6th ed. Philadelphia, 1998, Saunders.)
C
1078 PART IV ■ Obstetric Sonography
Later, because of differential growth, the yolk sac
comes to lie between the amnion and chorion. During
week 4, there is rapid proliferation and differentiation of
the syncytiotrophoblast, forming primary chorionic
villi. Traditional thinking that the syncytiotrophoblastic
cells invade the maternal endometrial vessels, leaving
maternal blood to bathe the trophoblastic ring, has been
challenged. Hustin
12
compared transvaginal imaging to
hysteroscopy of the placenta, chorionic villous sampling
tissue, and hysterectomy specimens with an early pregnancy in situ. Before 12 weeks, the intervillous space
contains no blood, only clear fluid, and on histologic
examination, the villous tissue is separated from the
maternal circulation by a continuous layer of trophoblastic cells. Only after the third month does the trophoblastic shell become broken and the maternal circulation
become continuous with the intervillous space. Further,
at weeks 8 and 9 of gestation, the trophoblastic shell
forms plugs within the spiral arteries, allowing only filtered plasma to permeate the placenta.
13
In two thirds of
abnormal pregnancies, the trophoblastic shell is thinner
and fragmented, and the trophoblastic invasion of the
spiral arteries is reduced or absent.
Vascularization of the placenta occurs at the begin-
ning of the fifth week. Oh et al.
14
15
showed significant
increases in sac size from 5 weeks onward in normal
pregnancies versus pregnancy failures. The rationale for
placental vascularization was based on early work by
Folkman,
16
who showed that tumors can grow to a size
of 3 mm being nourished only by diffusion. To exceed
this size, cells must recruit host blood vessels, or the cells
at the center will receive inadequate nutrition. Similarly,
the rapidly growing embryonic implantation must be
vascularized by the 3-mm stage that occurs at 5 weeks’
gestation.
During the fifth week, the embryo is converted by the
process of gastrulation from a bilaminar disk to a trilaminar disk with the three primary germ cell layers:
ectoderm, mesoderm, and endoderm. During gastrulation, the primitive streak and notochord form. The
primitive streak gives rise to the mesenchyme, which
forms the connective tissue of the embryo and stromal
components of all glands.
The formation of the neural plate and its closure to
form the neural tube is referred to as neurulation. This
process begins in the fifth week in the thoracic region
and extends caudally and cranially, resulting in complete
closure by the end of the sixth week (day 42). Failure of
closure of the neural tube results in neural tube defects.
During the fifth week, two cardiac tubes (the primitive heart) develop from splanchnic mesodermal cells. By
the end of the fifth week, these tubes begin to pump into
a primitive paired vascular system. By the end of the fifth
week, a vascular network develops in the chorionic villi
that connect through the umbilical arteries and vein to
the primitive embryonic vascular network.
Essentially all internal and external structures present
in the adult form during the embryonic period, which
ends at 10 menstrual weeks. By the end of the sixth week,
blood flow is unidirectional, and by the end of the eighth
week, the heart attains its definitive form. The peripheral
vascular system develops slightly later and is completed
by the end of the tenth week. The primitive gut forms
during week 6. The midgut herniates into the umbilical
cord from week 8 through the end of week 12. The
rectum separates from the urogenital sinus by the end of
week 8, and the anal membrane perforates by the end of
week 10. The metanephros, or primitive kidneys, ascend
from the pelvis, starting at approximately week 8, but do
not reach their adult position until week 11. Limbs are
formed with separate fingers and toes. Almost all congenital malformations except abnormalities of the genitalia originate before or during the embryonic period.
External genitalia are still in a sexless state at the end of
week 10 and do not reach mature fetal form until the
end of week 14.
Early in the fetal period, body growth is rapid and
head growth relatively slower, with the crown-rump
length doubling between weeks 11 and 14.
SONOGRAPHIC APPEARANCE OF
NORMAL INTRAUTERINE
PREGNANCY
Gestational Sac
Implantation usually occurs in the fundal region of the
uterus between day 20 and day 23.
implantation sites in 21 patients it was found that
implantation occurs most frequently on the uterine wall
ipsilateral to the ovulating ovary and least often on the
contralateral wall.
nant sleeping positions in the peri-implantation period,
Magann et al.
17
In addition, in a study of predomi-
18
found that the 33% of women who slept
prone were most likely to have a high or fundal implantation than those who slept on their back or side. The
latter groups predominantly had implantations corresponding to their resting posture.
At 23 days, the entire conceptus measures approximately 0.1 mm in diameter and cannot be imaged by
TAS or TVS techniques. The earliest sonographic sign
of an IUP was described by Yeh et al.,
a focal echogenic zone of decidual thickening at the site
1
of implantation at about
3
age. This sign is nonspecific and of limited diagnostic
value.
The first reliable gray-scale evidence of an IUP is
visualization of the gestational sac within the thickened
decidua. Yeh et al.
19
originally identified this sign,
referred to as the intradecidual sign (Fig. 30-5). An
intradecidual gestational sac should be eccentrically
17
In a study of early
19
who identified
to 4 weeks of gestational
2
Chapter 30 ■ The First Trimester 1079
β β
( )
÷
( )
=
A
FIGURE 30-5. Intradecidual sac sign. A, Sagittal scan at 4 weeks, 4 days shows implantation site as a 2-mm focal thickening
of posterior endometrium (arrow). The chorionic fluid in the sac is just barely visible. The mass slightly displaces the endometrial stripe
and has a slightly echogenic rim. B, Color Doppler image shows prominent terminal portion of a spiral artery (arrow) extending up to
the sac.
located within the endometrium and should abut the
endometrial canal. It is important to ensure that the sac
abuts the endometrial canal to distinguish an intrauterine gestational sac from a decidual cyst.
19
As a general rule, it is possible to demonstrate an early
1
4
IUP as a small intradecidual sac between
and 5
2
weeks’ gestational age using TVS (Fig. 30-6). Oh et al.
used a high-frequency (7.5-10 MHz) transvaginal transducer and were able to identify a gestational sac in all 67
patients scanned between 28 and 42 days’ gestational age;
mean sac diameter between 28 and 35 days was 2.6 mm.
In a literature review, Nyberg and Filly4 noted the
importance of the appropriate use of a threshold level
and a discriminatory level for the appearance of a gestational sac. The threshold level identifies the earliest one
can expect to see a sac (4 weeks, 3 days), and the dis-
criminatory level identifies when one should always see
the sac (5 weeks, 2 days). Although the menstrual history
provides useful information early in a woman’s obstetric
care, because of the variability in the timing of ovulation
and the unreliability of menstrual history, discriminatory
levels based on history are of limited clinical use. Discriminatory levels using the serum beta subunit of human
chorionic gonadotropin (β-hCG) provide a more reproducible value that can help guide management in clinical
practice.
The serum β-hCG level becomes positive shortly
after implantation, long before the gestational sac is
visualized sonographically. A disproportionately low
β-hCG is an indicator of a poor prognosis.
20
Although
many earlier studies (from the 1970s) use the Second
International Standard (IS) for serum β-hCG, the
World Health Organization (WHO) First International
B
Reference Preparation (IRP) has been developed more
recently and is in common usage. The IRP/IS preparations differ by a factor of approximately 2 : 1, although
this ratio varies among laboratories. To convert from
the Second IS to the First IRP, the following formula
can be used:
-hCG IRP -hCG nd IS
2 2
15
A gestational sac can often be visualized sonographi-
cally at low serum β-hCG levels. Extensive effort has
been made to identify a discriminatory level for the
serum β-hCG above which it is abnormal not to be able
to identify a gestational sac with ultrasound. Using TAS,
Nyberg et al.
21
demonstrated gestational sacs in 36/36
patients with normal IUP in whom serum β-hCG was
greater than 1800 mIU/mL (Second IS).
In a subsequent article by Nyberg et al.,22 TVS cor-
rectly identified intrauterine gestational sacs in 20% of
patients with β
-hCG levels below 500 mIU/mL (Second
IS), four of five patients with β-hCG levels of 500 to
1000 mIU/mL, and all 17 with β-hCG levels greater
than 1000 mIU/mL. Bree et al.23 identified a discriminatory level of 1000 mIU/mL (IRP) for TVS.
In a series of 60 patients whose ovulation was
timed by ultrasonic follicle monitoring, Sengoku et al.
24
assessed sac appearance, size, and levels of β-hCG.
Only 10 sacs were seen with a β-hCG of less than
1000 mIU/mL (IRP), five of six sacs with levels of 1000
to 2000 mIU/mL, and all sacs with levels above
2000 mIU/mL.
Keith et al.25 found that the β-hCG level above
which a singleton sac was always seen with TVS was
1161 mIU/mL (Third International Standard). This
1080 PART IV ■ Obstetric Sonography
A
C
FIGURE 30-6. Intradecidual sac sign. A, Transabdominal scan at 32 days. The small sac is not visualized in this scan. B and C,
Transvaginal scans the same day showing the echogenic ring of the sac (black arrow) implanted just below the endometrial interface (white
arrow). D,
Color Doppler flow of a feeding spiral artery adjacent to the sac with low-velocity flow of 10 cm/sec.
B
D
increased to 1556 mIU/mL in twins and 3372 mIU/mL
in triplets. When applying discriminatory levels in clinical practice, it is important to remember that the actual
discriminatory level depends of the (1) resolution of the
ultrasound scanner, (2) patient’s body habitus, (3) position of the uterus, and (4) type of hormonal assay.
Keith’s data emphasize that the use of discriminatory
levels in isolation to effect clinical decision making
ignores multifetal gestation. Discriminatory levels can be
used to guide management but cannot be used as absolute indicators that the absence of a sonographically
demonstrable gestation sac is abnormal. In a study of
pregnancies achieved by assisted reproductive techniques, Pellicer et al.
26
found that an embryonic sac
could be visualized at 37 to 38 menstrual days.
The double-decidual sign was previously described
by Nyberg et al.
27
as a method of differentiation between
an early IUP and the pseudosac of an ectopic pregnancy.
The endometrium in the pregnant state is actually called
the decidua capsularis, decidua vera, and decidua basalis
(Figs. 30-7, 30-8, and 30-9). The double-decidual sign
is based on visualization of the gestational sac as an
echogenic ring formed by the decidua capsularis and
chorion laeve eccentrically located within the decidua
vera (Fig. 30-7), forming two echogenic rings. The outer
ring is formed by the echogenic endometrium of the
lining of the uterus. The decidua basalis–chorion frondosum (future placenta) may also be visualized as an area
of eccentric echogenic thickening. The double-decidual
sign can usually be identified by about 5.5 to 6 weeks’
Chapter 30 ■ The First Trimester 1081
FIGURE 30-7 Double-decidual sign.
Diagram of anatomic basis showing three layers of
decidua and endometrial cavity. (From Lyons EA,
Levi CS. The first trimester. Radiol Clin North Am
1982; 20:259.)
FIGURE 30-8. Decidual layers. Sagittal transvaginal sono-
gram at 7 weeks shows the gestational sac (arrowhead) and the
maternal decidua (arrow) as separate echogenic bands.
gestational age, at approximately the same time that
the yolk sac becomes visible with TVS. A well-defined
double-decidual sign is an accurate predictor of the presence of an intrauterine gestational sac. A vague or absent
double-decidual sign may be seen in some patients with
a fluid-filled pseudosac associated with an ectopic pregnancy and should be considered nondiagnostic.
The double-decidual sign was originally described as
specific for an early IUP. Yeh et al.
19
clearly saw the
double-decidual sign in 30.6%, vaguely in 33.3%, and
1
3
not at all in 36.1% of IUPs at
to 7 weeks’ gestational
2
age. They identified a double-decidual sign in two of five
ectopic pregnancies, casting doubt on the usefulness of
this sign. In our experience, a clear double-decidual sign
is useful in predicting the presence of an IUP. A vague
or absent double-decidual sign is considered nondiagnostic. Parvey et al.
28
found a double-decidual sac in only
53% of early pregnancies with no yolk sac or embryo
present. They also assessed visualization of the echogenic
chorionic rim alone as a sign of IUP and found its
presence in 64% of cases. It was more clearly defined in
later pregnancies with a higher β-hCG level (mean,
A
C
e
c
B
FIGURE 30-9. Subchorionic hemorrhage. A, Transab-
dominal scan at 10 weeks. The sac and embryo are seen as well as
a fluid collection (arrow) behind the chorion, a subchorionic
hemorrhage. (arrow) B, Transvaginal sagittal and 3-D scans show
the fluid collections (arrows); e, embryo; c, chorion.
16,082 mIU/mL) and thin, less clearly defined or even
absent in the earliest pregnancies. The pseudo–gestational sac may occasionally appear as a double-decidual
sac or chorionic rim sign, but further scanning should
differentiate the two.
Using a higher-frequency 10-MHz transvaginal trans-
ducer in scanning patients who had a positive pregnancy
test and only a small (<
tion” seen with a 6- to 7-MHz transducer, Benacerraf
29
were able to improve their diagnostic confidence
et al.
1 cm) intrauterine “fluid collec-
1082 PART IV ■ Obstetric Sonography
in all eight patients with an IUP. This demonstrates the
need to scan transvaginally with a high-frequency transducer when an early pregnancy is in question.
The normal gestational sac is round in the very early
stages and implants immediately beneath the thin, echogenic endometrial stripe (see Fig. 30-6, C ). As it enlarges,
the sac often has a somewhat oval shape because of the
pressure exerted by the muscular uterine walls. It can be
distorted during the transvaginal examination by compressing the uterus with the vaginal probe. The gestational (or chorionic) sac is filled with extracoelomic or
chorionic sac fluid that is normally weakly reflective
and more echogenic than the amniotic fluid. This difference is best appreciated if the system gain is increased.
The low-level echoes within the chorionic fluid are
accentuated, and yet the amniotic fluid remains echo
30
(Fig. 30-10). The low-level echoes are likely caused
free
by the relatively thick proteinaceous material in chorionic fluid.
31
Transvaginal color flow Doppler sonography may
be helpful in identifying the presence of an early intrauterine gestational sac (see Figs. 30-5, B, and 30-6, D).
It has also proved helpful in distinguishing a normal
from a failed intrauterine gestation and in the detection
of an ectopic pregnancy through the exclusion of an
32
Emerson et al.32 found that the detection of peri-
IUP.
trophoblastic flow of high velocity and low impedance
increased the sensitivity of detection of IUP from 90%
to 99%. Even before a sac is seen, flows of 8 to 30 cm/
sec were found in the endometrium at the implantation
site. Parvey et al.
28
found that 15% of IUPs without the
presence of a sac had high-velocity, low-impedance,
AC
CC
SCH
FIGURE 30-10. Echogenicity of fluids. Transvaginal
sonogram of a 12-week sac with the echo-free amniotic fluid (AC),
mildly echogenic chorionic fluid (CC), and more echogenic blood
in the subchorionic space (SCH).
intradecidual arterial-type flow. A specificity and positive
predictive value of 95% could be achieved in diagnosing
an intrauterine gestation by using a peak systolic intradecidual flow velocity of 15 cm/sec or more and a resistive index (RI) of 0.55 or less. As mentioned previously,
however, use of Doppler ultrasound on the early gestational sac increases the amount of power deposition
compared to gray-scale imaging and therefore is infrequently used.
Yolk Sac
The yolk sac is the first structure to be seen normally
within the gestational sac. Using TAS, it is often seen
when the mean gestational sac diameter (MSD) is
10 to 15 mm and should always be visualized by an
MSD of 20 mm.33 Transvaginal techniques allow earlier
and more detailed visualization of the yolk sac (Fig.
30-11), which should always be visualized by an MSD
of 8 mm.
34
The demonstration of a yolk sac may be critical in
differentiating an early intrauterine gestational sac from
a pseudosac.
34
Although the double-decidual sign is not
100% specific for presence of an IUP, the identification
of a yolk sac within the early gestational sac is diagnostic
of IUP (Fig. 30-12). The yolk sac plays an important
role in human embryonic development.
1
While the placental circulation is developing, the yolk sac has a role
in transfer of nutrients to the developing embryo in the
third and fourth weeks. Angiogenesis (blood vessel formation) occurs in the wall of the yolk sac in the fifth
week. The mesenchymal cells or angioblasts aggregate to
form “blood islands”; a cavity forms within these islands,
which fuse with others to form networks of endothelial
channels. Vessels extend into adjacent areas by endothelial budding and fusion with other vessels. This vascular
network in the wall of the yolk sac eventually joins the
fetal circulation via the paired vitelline arteries and veins
through a stalk called the vitelline duct. Hematopoiesis
(blood cell formation) occurs first in the well-vascularized extraembryonic mesoderm covering the yolk sac
wall in the fifth week, in the liver in the eighth week,
and later in the spleen, bone marrow, and lymph nodes.
The dorsal part of the yolk sac is incorporated into the
embryo as primitive gut (foregut, midgut, and hindgut)
in the sixth week. The yolk sac remains connected to the
midgut by the vitelline duct. In some cases the vitelline
duct can be demonstrated sonographically (Figs. 30-13
and 30-14).
Lindsay et al.
35
reported that the yolk sac grows at a
rate of 0.1 mm per millimeter of MSD growth when the
MSD is less than 15 mm, then slows to 0.03 mm. The
upper limit of normal for yolk sac diameter between 5
and 10 weeks of gestational age is 5.6 mm.
The number of yolk sacs present can be helpful in
determining amnionicity of a multifetal pregnancy (Fig.
30-15). In general, if the embryos are alive, the number
Chapter 30 ■ The First Trimester 1083
A
C
FIGURE 30-11. Early sac and embryo. A, Transverse transvaginal sonogram of the anteverted uterus (UT) demonstrates a small
gestational sac at 4 weeks, 3 days. B, Sonogram at 5 weeks, 6 days shows an enlarging gestational sac with the appearance of a 2-mm yolk
sac (arrow). C, Magnified view of the sac reveals a 2.5-mm embryo (calipers); CRL, crown-rump length. D, M-mode ultrasound shows
cardiac motion at a fetal heart rate (FHR) of 107 beats/min (arrow).
B
D
A
FIGURE 30-12. Normal yolk sac. A, Nine weeks. B, Eight weeks.
B
1084 PART IV ■ Obstetric Sonography
ys
Visualization of the vitelline arteries and veins is possible on the vitelline duct and should be possible on the
periphery of the yolk sac itself. A magnified 9 weeks sac
shows irregularities in the wall of the yolk sac that correspond to the arteries (Fig. 30-16).
e
FIGURE 30-13. Normal embryo at 8 weeks. Trans-
vaginal sonogram shows vitelline duct (arrow), yolk sac (ys), and
embryo (e).
VD
YS
Chorion
Subchorionic bleed
FIGURE 30-14. Vitelline duct. Three-dimensional (3-D)
ultrasound image of an embryo at 8 weeks with the vitelline duct
(VD) connecting to the yolk sac (YS). There is also a subchorionic
hemorrhage.
of yolk sacs and the number of amniotic sacs are the
same. In a monochorionic monoamniotic (MCMA)
twin gestation, there will be two embryos, one chorionic
sac, one amniotic sac, and one yolk sac. Levi et al.
36
examined four MCMA twin pregnancies, all with a
single yolk sac. One was a conjoined twin and one a twin
ectopic, with both pregnancies terminated. The other
two pregnancies delivered normally at 34 weeks. Of
the four cases, two had a larger-than-normal yolk sac
5.6 mm), and two had a normal sac. Therefore, in
(>
MCMA twins, a single, large, or normal-sized yolk sac
with two live embryos can result in a normal twin
delivery.
Embryo and Amnion
Yeh and Rabinowitz37 described the double-bleb sign as
the earliest demonstration of the amnion. The two blebs
represent the amnion and yolk sac and can be identified
1
5
as early as
weeks when the crown-rump length
2
(CRL) is 2 mm. At that point, the embryonic disk is
situated between the yolk sac and amnion. However,
although visualization of the tiny (<
2 mm) bleb of
amnion may occur before visualization of the embryo,
this is a transient phenomenon. Visualization of the
amnion in the absence of an embryo usually occurs in
intrauterine embryonic death as a result of resorption of
the embryo (Fig. 30-17).
Amniotic fluid initially is a colorless, fetal dermal transudate; as the skin cornifies and the kidneys begin to
function, at about 11 weeks, it becomes pale yellow.
Birnholz and Madanes
volume after subtracting the estimated volume of the
embryo.
30
The amnion becomes visible when the embryo
30
calculated the amniotic fluid
has a CRL of 2 mm at 6 weeks. The cavity becomes almost
spherical by about 7 weeks, likely a result of the more
rapid increase in fluid volume relative to the growth of
the sac membrane to accommodate it. The actual rate of
fluid increase is more rapid after about 9 weeks, when fetal
urine is produced. Fluid accumulates at about 5 mL (cc)
per day at 12 weeks’ MA. The amniotic cavity expands to
fill the chorionic cavity completely by week 14 to 16. It
is normal to identify the amnion as a separate membrane
or sac within the chorionic cavity before 14 to 16 weeks
(Fig. 30-18). Occasionally, the amnion and chorionic
membranes may fail to fuse at week 16, and separation of
these membranes may persist for a short time.
Iatrogenic or spontaneous rupture of the amniotic
membrane is a rare occurrence and even more rarely
results in the amniotic band sequence. This rupture
may result in retraction of the amnion in part or in
whole, up to the base of the umbilical cord where the
two membranes are adherent. More often, the floating
amniotic membranes do not adhere to the fetus, and no
fetal anomalies occur.
Embryonic Cardiac Activity
Using TVS, an embryo with a CRL as small as 1 to
2 mm may be identified immediately adjacent to the
yolk sac (Fig. 30-19). In normal pregnancies the embryo
can be identified in gestational sacs as small as 10 mm4
and should always be identified when the MSD is 16 to
18 mm or larger with optimal scanning parameters and
high-resolution TVS.
38
Chapter 30 ■ The First Trimester 1085
A
FIGURE 30-15. Six-week monochorionic diamniotic (MCDA) twins. Two separate yolk sacs are seen within a single
gestational sac at 6 weeks on 2-D (A) and 3-D (B) images.
A
B
B
C
FIGURE 30-16. Normal yolk sac and vitelline duct. Transvaginal scans of 9-week pregnancy focusing on the yolk sac (A)
and flow within the vitelline duct (B and C).
1086 PART IV ■ Obstetric Sonography
Embryologic data suggest the tubular heart begins
to beat at 36 to 37 days’ gestational age.
McAlpin
sac before visualization of the embryo at the end of
the fifth week. Ragavendra et al.
39
described cardiac activity adjacent to the yolk
40
1
Cadkin and
placed a 12.5-MHz
endoluminal catheter transducer into the endometrial
+
+
canal adjacent to the gestational sac. They identified
cardiac activity in an embryo with a CRL of 1.5 mm and
resolved the two walls of the heart, seen only as a tube.
Using TVS, absent cardiac activity may be normal in
embryos of less than 4 to 5–mm CRL. In general, cardiac
activity can be visualized in normal embryos of greater
than 5-mm CRL. Normal embryonic cardiac activity is
greater than 100 beats per minute (Video 30-1).
Umbilical Cord and Cord Cyst
The umbilical cord is formed at the end of the sixth week
(CRL =
4.0 mm) as the amnion expands and envelops
the connecting stalk, the yolk stalk, and the allantois.
The cord contains two umbilical arteries, a single umbilical vein, the allantois, and yolk stalk (also called the
omphalomesenteric duct or vitelline duct), all of which
AM
FIGURE 30-17. Monochorionic and diamniotic
twins with one intrauterine embryonic death and
one alive. Transvaginal sonogram at 10 weeks. On the left the
arrow is pointing to one of two adjacent sacs, one is the amnion
and the other the yolk sac. To the right is a single yolk sac (calipers)
with the live embryo not in the scan plane. Both embryos went
on to abort.
A
FIGURE 30-18. Normal 9-week embryo/amnion.
Normal separation of amnion (arrow) and chorionic sacs at 9
weeks. Transvaginal sonography shows the embryo (calipers) and
the amnion (AM).
B
FIGURE 30-19. Normal 6-week embryo. A, Image shows 6-week embryo (calipers) adjacent to the yolk sac. B, M-mode ultra-
sound shows a heart rate of 141 beats/min.
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