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J. Miravet-Valenciano et al.
28. Moreno I, Cicinelli E, Garcia-Grau I, GonzalezMonfort M, Bau D, Vilella F, etal. The diagnosis
of chronic endometritis in infertile asymptomatic
women: a comparative study of histology, microbial cultures, hysteroscopy, and molecular microbiology. Am J Obstet Gynecol. 2018;218(6):602.
e1–602.e16.
List of Relevant Websites
E-tegrity: http://www.etegritytest.com/
EFT®: http://klimanlabs.yale.edu/infertility/eft/
ERA: https://www.igenomix.com/tests/
endometrial-receptivity-test-era/
Part VII
Ultrasound and Pregnancy
Early Pregnancy Ultrasound
LauraDetti
23
Introduction
Early pregnancy ultrasound is performed to
assess the location of a pregnancy (intrauterine or
extrauterine) and its viability. It also appraises
the number of embryos and their chorionicity and
amnionicity and often is instrumental in predicting the development, and dictates the management, of a pregnancy in the second and third
trimester. Among the main objectives of the early
pregnancy ultrasound are correct dating, evaluation of early pregnancy landmarks and placental
location, and distinguishing normal from abnormal pregnancy. In addition, rst trimester ultrasound allows evaluation of the ovaries and the
corpus luteum.
Temporally, the rst structure to be appreciated by ultrasound is the gestational sac, followed
by the yolk sac, the embryo, and, when present,
the embryonal cardiac activity. There is general
consensus that the best technique to assess the
early pregnancy is by transvaginal ultrasound:
the higher resolution and the closer proximity of
the transvaginal transducer allow the identication of structures such as a 2-mm gestational sac,
or a 1-mm yolk sac, in addition to allowing excellent anatomical details of the embryo. In this
L. Detti (*)
University of Tennessee Health Science Center,
Department of Obstetrics and Gynecology,
Memphis, TN, USA
e-mail: ldetti@uthsc.edu
chapter we will describe the evaluation of the rst
trimester singleton and multiple pregnancy using
the transvaginal ultrasound technique.
Pregnancy Location
It is of foremost importance to locate a pregnancy
in a woman with a positive pregnancy test. An
intrauterine pregnancy can be identied with a
β-hCG level as low as 1500mIU/ml, depending
on the ultrasound machine capabilities. A conservative discriminatory β-hCG level of 3000mIU/
ml has been set forth by the American Institute of
Ultrasound in Medicine and the Society of
Radiologists in 2012 [1]. Based on these societies’ panel, presumptive treatment for ectopic
pregnancy with the use of methotrexate or other
pharmacologic or surgical means should be
undertaken only if a single β-hCG measurement
is greater than 3000mIU/ml. Under this condition, a viable intrauterine pregnancy is possible
but unlikely, and treatment can be initiated, especially if a repeat β-hCG level conrms the rst
one. The American College of Obstetrics and
Gynecology has recently endorsed this conservative approach without giving a specic discriminatory β-hCG level, as each institution should
have their own based on the level of expertise, as
well as laboratory thresholds, and ultrasound
capabilities [2].
© Springer Nature Switzerland AG 2019
L. A. Stadtmauer, I. Tur-Kaspa (eds.), Ultrasound Imaging in Reproductive Medicine,
https://doi.org/10.1007/978-3-030-16699-1_23
369
370
L. Detti
A true gestational sac within one side of the
endometrial echo is a reliable sign of intrauterine
pregnancy; however, an astute clinician must
always have concern for life-threatening concurrent ectopic pregnancy (heterotopic) or pregnancy loss. In the presence of an uncertain
situation, the clinician must decide what signs
and symptoms are normal or abnormal in early
pregnancy.
Embryonal Landmarks
andTemporal Appearance
Transvaginal ultrasound (TUS) features highresolution images, low interobserver variability,
and high reliability and is conventionally used to
make diagnosis of intrauterine pregnancy and to
follow up with its development. Gestational sac,
yolk sac, crown-rump length, heart rate, and
amniotic sac are the features evaluated to assess
the early pregnancy.
Gestational Sac (GS)
It is the rst structure to develop from the
implanted embryo, and it is present as early as 4
complete weeks’ gestation. By TUS, it can be
visualized as an echoic ring (trophectoderm) surrounding an anechoic center (uid), embedded in
one side of the endometrium (eccentric).
Typically, it is measured by averaging the three
diameters in the two orthogonal planes (Hellman’s
method), but more recently it is measured by only
the largest diameter (Rempen’s method). The
algorithm in the individual ultrasound machines
will calculate the gestational age based on one of
the two methods. Figure23.1 shows the correct
measurement of a GS based on three diameters in
the two orthogonal planes. The GS’s average
diameter grows linearly during the rst 12weeks
of pregnancy. This trend has been conrmed by
cross-sectional [3], as well as longitudinal [4],
studies. Figure23.2a shows the GS growth based
on longitudinal data from 193 pregnancies that
ended in live birth.
Yolk Sac (YS)
The secondary YS is the second structure to
develop, together with the embryo; however, in
most instances it is the rst of the two to be visualized. It should always be visualized when the
GS is greater than 8 mm in diameter [5]. It is
Fig. 23.1 Measurement of a gestational sac in the two orthogonal planes. Six weeks and 3days– normal GS
Gestational Sac Yolk Sac
Crown-Rump Length (mm)
OngoingOngoing
ab
cd
23 Early Pregnancy Ultrasound
371
6
5
4
3
2
1
0
45678
GS Average Diameter (cm)
Gestational age (weeks)
910
Ongoing
5
4
3
2.2
2
1
Diameter (mm)
0
5
3
2.7
2.6
678910
Gestational age (weeks)
Ongoing
3.8
4.4
Crown-Rump Length Heart Rate
40
30
20
10
0
5 678910
−10
Gestational age (weeks)
200
160
120
80
40
Heart Rate (BPM)
0
5 67 8910
Gestational age (weeks)
Fig. 23.2 Ultrasonographic measurement of various parameters during the rst 10 weeks of pregnancy. (a) Gestational
Sac; (b) Yolk Sac; (c) CRL, or Crown-Rump Length; (d) Heart Rate
ab
Fig. 23.3 (a) Correct measurement of the yolk sac. (b) A misshapen yolk sac
measured placing the cursor from the inner rim to
the opposite inner rim, and, if misshapen, the
Embryo andCrown-Rump Length
(CRL)
three dimensions in the two orthogonal planes
should be averaged. The YS grows linearly during the rst 10weeks of pregnancy, 0.44mm per
week (Fig.23.2b) [6], and is then progressively
distanced from the embryo by the developing
amniotic sac. Figure 23.3 shows a normal YS
with the correct measurement (a) and a misshapen YS (b).
The embryo develops together with the secondary yolk sac; however, because of its discoid
shape and the adjacent yolk sac, it is not easily
visualized until almost 6 weeks’ gestation.
Between 5 and 6 complete weeks’ gestation, the
embryo assumes a tubular shape, and, as the neural tube is sealed on both ends, it gradually
372
ab
L. Detti
assumes a C-shaped conformation. At this time
the amniotic sac becomes visible as a translucent
membrane projecting from the embryo’s stalk
within the GS.Until 53days (=9.4weeks’ gestation), the caudal portion of the embryo is the
tail. Only after 60days (=10.5weeks’ gestation)
does the head become the most cephalad portion
of the embryo/fetus. This means that until
11 weeks’ gestation, we measure the longest
fetal diameter rather than the real
CRL. Nonetheless, measuring the CRL is the
most reliable way to date a pregnancy when the
last menstrual period is not known. In addition,
when in the rst trimester the estimated gestational age by CRL differs greater than ±7days
from the gestational age by LMP, the estimated
date of delivery should be changed.
From 6 to 9.4weeks, the CRL grows approximately 1 mm/day [3, 4], as seen in Fig. 23.2c.
Figure23.4 shows an ultrasound picture (a) and
an electronic microscopy picture (b), of an
embryo at 5 weeks’ gestation. As seen, the
embryo is still discoid and the secondary YS is
adjacent to the embryo. Figure 23.5 shows the
Fig. 23.4 Ultrasound (a) and electronic microscopy (b) images of a 5weeks’ gestation embryo
ab
Fig. 23.5 Measurement of the CRL at 6 weeks and 3 days’ (a) and at 8weeks’ gestation (b)
23 Early Pregnancy Ultrasound
Fig. 23.6 M-mode for measurement of embryonal heart rate at 6weeks and 4days’ gestation
373
correct CRL measurement and the embryonal
stalk at 6weeks’ and at 8weeks’ gestation.
Embryonal Heart Rate (EHR)
The heart starts contracting to propel blood
before it is fully formed during the third week of
embryonal life or 5weeks’ gestation. The rate of
its contractions (beats per minute = BPM) is
slow in the beginning, and it progressively
increases until 8 complete weeks, when it
reaches approximately 180 BPM [7]. Between 5
and 6weeks, the EHR is about 100 BPM; however, it could be slower (Fig.23.2d). Figure23.6
shows the M-mode technique to measure the
EHR. The Doppler technique to measure the
EHR should not be used until after the completion of the rst trimester of pregnancy, to avoid
overheating of the delicate embryonal structures
and possible development of congenital defects
and/or intrauterine growth restriction [in accordance with the as low as reasonably achievable
(ALARA) principle] [8]. EHR increases exponentially from 5 to 8 complete weeks’ gestation,
and it then decreases to reach a plateau of 140–
150 BPM at 15weeks’.
Pregnancy Dating
Of the parameters previously described, the only
one that has proven reliability and reproducibility
to determine a pregnancy’s age is the CRL.When
an EHR is present, the CRL measurement can
reliably diagnose the gestational age. However, if
EHR is absent and the CRL measures less than
7mm (7weeks’ gestation), it becomes critical to
assess the presence of the AS. Since the AS
becomes visible on ultrasound at 7weeks’ gestation, even if the CRL measures 5 or 6 complete
weeks’ gestation, the presence of an AS would
date a pregnancy at least at 7weeks’. Figure23.7
shows an example of a pregnancy lost at 7weeks
and 2days, with the CRL measuring 5.6mm: the
CRL would date the pregnancy at 6weeks and
3days; however, the presence of the AS dates the
pregnancy to after 7weeks’. The “double-bleb”
sign, initially described as a sign of genetically
abnormal pregnancy, actually represents the yolk
374
Fig. 23.7 The double-bleb sign made of the yolk sac and
the amniotic sac with a faintly visualized embryo in
between
sac (left “bleb”) and the AS (right “bleb”) with
the embryo faintly visualized in between. These
ndings characterize a new concept of growth
restriction in the rst trimester, which could be
important in establishing the causes of a
pregnancy loss, especially in the instance of
recurrent early pregnancy loss.
Diagnosis ofPlacental Location
During implantation, the embryo penetrates
the functional layer of the endometrium with
the inner cell mass facing its basal layer. Upon
contact, the cytotrophoblast, the outer cell
layer of the blastocyst, starts proliferating to
create the trophoblastic shell. This shell is
comprised of a cytotrophoblast layer with
intermingled syncytial cells, which then
coalesce to form the syncytiotrophoblast [9].
During the third week of embryo development,
or 5weeks gestation, the cytotrophoblast and
syncytiotrophoblast form the villous chorion.
At this point, embryonic blood begins to ood
the villi via the umbilical arteries through the
embryonal stalk, which will progressively
elongate to form the umbilical cord. The
embryonal blood causes development of the
chorionic villi located above the basal decidua,
which will then anchor the chorion frondosum
with the apposed amnion.
L. Detti
Traditionally, placental location is identied
by TUS after 8weeks gestation, when the placenta forms by anchoring the chorion frondosum
with the apposed amnion in the basal decidua
[10]. The circulation in the chorion frondosum
starts becoming prominent, thus appearing
hyperechogenic on ultrasound and allowing its
localization in relationship to the uterine wall
[11]. Placental location has also been visualized
using power Doppler before 10weeks of gestation, at which point scattered vessels can be
identied surrounding the gestational sac [12].
However, identication of embryonal stalk, and
thus future location of the chorion frondosum
and the placenta, is possible via ultrasound by
5–6weeks gestation, and its reliability has been
conrmed by a pioneer study by our group [13].
In fact, placental location diagnosed at 5 or
6 weeks of gestation was consistent with the
location on mid-pregnancy ultrasound in 100%
of the 111 singleton and twin pregnancies studied, even if in 21.2% of the cases the placenta
had moved to an adjacent location (i.e., from
fundal, it became anterior or posterior by the
second trimester scan). Figure 23.8 shows placental location diagnosis on the two orthogonal
planes, and Fig. 23.9 shows 3D renderings of
6 weeks and 3 days and 7 weeks and 5 days
pregnancies.
Placental location has a signicant impact on
pregnancy outcome and on maternal and fetal
morbidity and mortality. Early identication of
placenta previa allows clinicians to more closely
follow the pregnancy, thus reducing risk of low
neonatal weight, postpartum hemorrhage, gestational hypertension, and preterm labor and delivery [11, 14, 15]. In the case of cesarean section
scar pregnancies, which are on the rise with
increasing incidence of cesarean deliveries and
which constitute 6.4% of ectopic pregnancies
[16], the risk of morbid adherence to the anterior
wall of the uterus and the posterior wall of the
bladder is considered so high that termination of
pregnancy is recommended [17]. Thus, early
knowledge of placental location allows the clini-
23 Early Pregnancy Ultrasound
375
Fig. 23.8 Antero-left placenta at 5weeks and 1day pregnancy. CP, chorionic plate
Fig. 23.9 3D renderings of an intrauterine pregnancy at 6 weeks and 3 days’ (a) and one at 7 weeks and 5 days’ gesta-
tion (b)
cian to identify potential risks and counsel the
patient accordingly. Similarly, knowing the site
of the placenta in the presence of uterine subseptations can help in counseling the patient about
the possible pregnancy outcome. Figure 23.10
shows a subseptate uterus with the GS on the
right of the subseptation and the placenta
implanted in the right lateral wall.
376
Fig. 23.10 Subseptate uterus with the GS on the right of
the subseptation and the placenta implanted in the right
lateral wall
Pregnancy Viability
Early pregnancy loss, or failed pregnancy, or miscarriage is dened as a nonviable, intrauterine
pregnancy with either an empty gestational sac or
a gestational sac containing an embryo or fetus
without fetal heart activity within the rst 12 complete weeks of gestation [18]. It is the most common complication of early pregnancy, affecting as
many as 30% of pregnancies following assisted
reproduction technology [19]. In spontaneous
pregnancies, the reported incidence of miscarriage
is lower, about 10% [20, 21]. The difference is
probably due to the fact that spontaneous pregnancy is clinically recognized at a later time than
assisted reproduction ones, and an early miscarriage is easily missed. Vaginal bleeding is a common sign of early pregnancy failure; however, it
can be confused with a delayed menstruation and
remains undiagnosed. Chromosomal abnormalities are the cause of a miscarriage in greater than
50% of the times, and aneuploidy is the most frequently observed abnormality [22, 23]. Changes in
the ultrasound features have been alternatively
investigated to predict pregnancy outcome and in
particular miscarriage. Logistic regression models
including large numbers of pregnancies identied
maternal age, HR, CRL, and vaginal bleeding as
the most signicant prognostic variables to predict
a miscarriage in both spontaneous [24] and invitro
fertilization pregnancies [25]. However, the models were not specic for a denite gestational age
L. Detti
and included parameters, such as maternal age,
which, alone, is a well-established risk factor for
rst trimester miscarriage [26]. A recent systematic review summarized sensitivities and specicities for the ultrasound parameters and found an
EHR ≤110 BPM to be the most reliable one to
predict a subsequent miscarriage, with a sensitivity of 68.4%, a specicity of 97.8%, a positive
likelihood ratio of 31.7 (95% condence interval
12.8–78.8), and a negative likelihood ratio of 0.32
(95% condence interval 0.16–0.65) [27]. In
women with an HR≤110 BPM and vaginal bleeding, all the statistics increased, indicating enhanced
predictability. It was also reported that, in addition
to CRL, GS, and EHR, below the 5th percentile, a
YS diameter above the 95th percentile was predictive of early miscarriage (odds ratio 1.04); however, a normal YS did not decrease the risk of
miscarriage, if the other parameters were abnormal [28]. Other studies have indicated an enlarged
YS to be associated with miscarriage, while an
abnormal YS shape was not predictive [5, 29, 30].
All the markers established as predictors of
adverse pregnancy outcomes, however, have
always been evaluated cross-sectionally with only
one ultrasound per patient [5, 24, 25, 27–30]. Our
group performed a longitudinal study of all the
early pregnancy landmarks. In this study multiple
ultrasounds were performed to accurately represent all gestational ages in each patient. This
allowed us to obtain longitudinal data in the same
patient, further strengthening our study. We previously described a nomogram of YS development
during the rst 10weeks of pregnancy with serial
ultrasounds (Fig.23.11a) [6]. After 5weeks’ gestation, the YS reliably detects pregnancies that
will end in miscarriage. In these pregnancies, the
YS was either smaller or larger than in ongoing
pregnancies. While all pregnancies with large YS
miscarried within 10 weeks, some pregnancies
with smaller YS miscarried beyond the rst
10 weeks of pregnancy. In a subsequent study
which combined all rst trimester parameters, the
same group established that YS and GS are the
earliest parameters that can be reliably used as a
prognostic factor for poor pregnancy outcome
later in the rst trimester, as they become abnormal as early as 6weeks of gestation, even if the
actual loss occurs after 8weeks [4]. Figure23.11
shows the changes of the early pregnancy land-