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2 Basics ofThree-Dimensional Ultrasound andApplications inReproductive Medicine
37
Fig. 2.11 (continued)
Conclusions
Three-dimensional US opens up new clinical
applications and facilitates many of the procedures originally performed with 2D US.Threedimensional US offers some features not
available with 2D US; this includes measurements in 3D space– including volume calculations– with high accuracy, even for non-regular
shaped structures, display of an arbitrary section,
and displaying a 3D image. Currently, in most
fertility clinics, 3D US is not a diagnostic armamentarium, although it has become an indispensable tool in many specialty elds, such as prenatal
diagnosis, neurology, or cardiology. However,
we are witnessing a still growing interest in this
stunning technique being implemented in many
research settings within the scope of gynecology
and reproductive medicine. Nowadays, within
the scope of fertility therapy, 3D US has already
become established as the preferred method for
diagnosing uterine malformations. It may also
play an increasingly important role in the near
future when it comes to the accurate diagnosis of
PCOS, in the assessment of ovarian reserve, and
in estimating the risk of OHSS.Thus, 3D US will
become one of the decision-making factors in
choosing the optimal stimulation protocol and in
monitoring follicular development, an area where
3D applications have the potential for optimizing
the IVF process and setting benchmarks for standardization, i.e., in the process of COS.
When 3D US data is acquired, the information
can be stored for documentation (which might be
needed for future therapy planning and most
important for legal reasons) or post-processing. It
can be easily shared for an expert review, interdisciplinary consultation, teaching, and/or telemedicine. Additionally, data can be sent between
IVF centers and the attending gynecologist,
38
M. Murtinger and M. Schu
which is most important for a patient-friendly
therapy. Thereby, data can be transferred through
a secured connection via a PACS server and virtual private network (VPN) tunneling, and the
corresponding medical software allows seamless
integration of all processes needed for an accurate and precise workow [81].
Meanwhile, there are various post-processing
modalities available. However, a lack of standardization, the time needed for post-processing,
and operators who are often insufciently trained
are still obstacles to a broader application of 3D
US and its use in a clinical setting. This last point
is of particular importance, since the application
of 3D techniques denitely needs extensive training and a learning curve [82]. There is a clear
trend toward rapid increasing processing power,
improved image quality, and more user-friendly
instruments and software. However, manufactures should be encouraged to provide training
modules and more user-friendly software for
post-processing to allow a higher acceptance of
3D US techniques. Additionally, the implementation and usage of portable 3D US systems might
possibly accelerate the application of 3D
US.Thus, there is no doubt that new innovation
will offer new application areas even within ART.
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Two-Dimensional andThreeDimensional Doppler
inReproductive Medicine
ErnestHungYuNg
3
Introduction
In vitro fertilization-embryo transfer (IVF-ET) is
an effective treatment for various causes of infertility and involves the development of multiple
follicles, oocyte retrieval and embryo transfer
after fertilization. Multiple embryos are still
being replaced in order to compensate for their
low implantation potential, which have remained
steady at 30% for a long time. The development
of multiple follicles in response to gonadotrophin
stimulation is considered as the key factor leading to successful outcome. Successful implantation is dependent on interaction between a good
quality embryo and a receptive endometrium.
Ultrasound examination is essential during
IVF for predicting and monitoring the ovarian
response to gonadotrophin, assessing the endometrium, guiding the transvaginal aspiration of
oocytes and transferring embryos to the uterine
cavity. Angiogenesis plays a critical role in various female reproductive processes such as the
development of a dominant follicle, formation of
a corpus luteum, growth of endometrium and
implantation [1, 2]. This chapter covers the use of
two dimensional (2D) and three dimensional
E. H. Y. Ng (*)
Department of Obstetrics and Gynaecology, The
University of Hong Kong, Hong Kong, SAR, China
e-mail: nghye@hku.hk
(3D), in particular the role of endometrial and
subendometrial blood ow determined by
Doppler ultrasound in predicting the IVF success
and the role of ovarian stromal blood ow determined by Doppler ultrasound in predicting ovarian response.
Endometrial Blood Flow
Ultrasound examination of the endometrium provides a noninvasive evaluation of the endometrium during IVF [3]. Ultrasound parameters of
endometrial receptivity include endometrial
thickness, endometrial pattern, endometrial volume and Doppler study of uterine arteries and the
endometrium. Endometrial thickness and pattern
have low positive predictive value and specicity
for the IVF outcome [4, 5], whereas endometrial
volume measured by 3D ultrasound is not predictive of pregnancy [6–9].
Assessment of endometrial blood ow adds a
physiological dimension to the anatomical ultrasound parameters. A good blood ow towards the
endometrium is usually considered as an essential requirement for successful implantation.
Jinno et al. [10] measured endometrial tissue
blood ow in infertile women by the intrauterine
laser Doppler technique between days 4 and 6 of
the luteal phase of a spontaneous cycle preceding
IVF. The IVF pregnancy rate was signicantly
higher in women with endometrial tissue blood
© 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_3
43
44
E. H. Y. Ng
ow of at least 29mL/min per 100 gm of tissue
than in women with lower values (42% vs 15%,
respectively, P<0.05).
Endometrial blood ow starts from the radial
artery, which divides after passing through the
myometrial-endometrial junction to form the
basal arteries that supply the basal portion of the
endometrium and the spiral arteries that continue
up towards the endometrium. Endometrial blood
ow can be determined by colour and power
Doppler ultrasound. Power Doppler imaging is
more sensitive than colour Doppler imaging at
detecting low velocity ow and hence improves
the visualization of small vessels [11]. In combination with 3D ultrasound, power Doppler provides a unique tool with which to examine the
blood ow of both endometrial and subendometrial regions.
Blood Flow ofUterine Vessels
Doppler study of uterine vessels reecting downstream impedance to ow has been assumed to
reect the blood ow towards the endometrium.
It is usually expressed as the pulsatility index (PI)
and the resistance index (RI) (Fig.3.1). PI is calculated as the peak systolic velocity (PSV) minus
end-diastolic velocity divided by the mean,
whereas RI is the ratio of PSV minus enddiastolic velocity divided by PSV.
Flow velocity waveforms are obtained from
the ascending main branch of the uterine artery
on the right and left side of the cervix in a longitudinal plane before it enters the uterus. The
‘gate’ of the Doppler is positioned when the vessel with good colour signals is identied on the
screen. The PI and RI of the uterine arteries were
calculated electronically when three similar, consecutive waveforms of good quality were
obtained.
Good uterine blood ow as shown by low PI
or RI is correlated with successful IVF outcomes
[12, 13]. Steer etal. [12] classied PI measured
on the day of ET as low, medium and high in the
ranges of 0–1.99, 2.00–2.99 and ≥3.00, respectively, and reported a 35% implantation failure
when PI was >3.0. Using a PI upper limit of 3.0
[12] or 3.3 [13], the uterine Doppler ow indices
have a high negative predictive value and sensitivity (in the ranges of 88–100% and 96–100%,
respectively) and a relatively higher range of
positive predictive value and specicity (44–56%
and 13–35%, respectively) when compared with
endometrial thickness and pattern [5].
Uterine artery Doppler study may not reect
the actual blood ow to the endometrium as the
major compartment of the uterus is the myometrium, and there is collateral circulation between
uterine and ovarian vessels. I have shown that
2D Doppler study of uterine vessels is a poor
reection of subendometrial blood ow by 3D
power Doppler in both stimulated and natural
cycles as endometrial and subendometrial 3D
Doppler ow indices were similar among
patients with averaged uterine PI <2.0, 2.0–2.99
and ≥3.0 [14].
Endometrial andSubendometrial
Blood Flow by 2D Doppler
Endometrial and subendometrial blood ow
examined by colour (Table 3.1) and power
Doppler (Table3.2) were correlated with implantation or pregnancy rates of IVF. 2D Doppler
ow indices of spiral arteries such as PI and PSV
are not predictive of pregnancy [8, 15, 16],
although Battaglia etal. [17] and Kupesic etal.
[18] found signicantly lower spiral artery PI in
pregnant cycles than non-pregnant cycles.
Yang et al. [19] used a computer software to
measure the area and intensity of colour signals
present in the endometrium in a longitudinal axis,
i.e. intraendometrial power Doppler area (EDPA).
Signicantly higher EDPA was found in pregnant
cycles than non-pregnant cycles (8.8 mm
5.8 mm2, respectively). Patients with EDPA
<5 mm2 had signicantly lower pregnancy rate
(23.5% vs 47.5%; P = 0.021) and implantation
rate (8.1% vs 20.2%; P=0.003) than those with
≥5mm2. Contart etal. [20] graded endometrial
blood ow by the visualization of power Doppler
in the quadrants in the fundal region of the transverse plane but could not demonstrate any predictive value of such grading system.
2
vs
3 Two-Dimensional andThree-Dimensional Doppler inReproductive Medicine
a
45
b
Fig. 3.1 (a, b) Uterine blood ow measured by 2D Doppler ultrasound
46
Table 3.1 Summary of studies of endometrial blood ow by 2D colour Doppler
Study IVF cycles USS parameters
Zaidi etal.
(1995) [15]
Battaglia
etal. (1997)
[17]
Chien etal.
(2002) [21]
USS ultrasound, PI pulsatility index, PSV peak systolic velocity, OR oocyte retrieval, ET embryo transfer
Table 3.2 Summary of studies of endometrial blood ow by 2D power Doppler
Study IVF cycles USS parameter
Yang etal.
(1999) [19]
Yuval etal.
(1999) [16]
Contart etal.
(2000) [20]
Schild etal.
(2001) [26]
MaugeyLaulom etal.
(2002) [22]
USS ultrasound, PI pulsatility index, PSV peak systolic velocity, OR oocyte retrieval, ET embryo transfer
96cycles using a
long protocol
60cycles Uterine and spiral PI OR Uterine and spiral PI lower in pregnant
623cycles using
ultrashort and
ultralong protocols
95cycles using long
and short protocols
Endometrium
≥10mm
156cycles using a
long protocol
185cycles using a
long protocol
135cycles using a
long protocol; rst
cycle only
144cycles using a
long protocol
Spiral PI and PSV hCG No difference in subendometrial PI and
Presence of endometrial and
subendometrial ow
Presence of endometrial
blood ow
Uterine and spiral PI and RI ET Signicantly lower implantation and
Presence of endometrial and
subendometrial (<10mm)
blood ow Presence of subendometrial ow 5.9
Intraendometrial power Doppler
area (EDPA)
2
<5mm
PI and RI OR
Fundal region along transverse
plan
Grades I, II, III and IV
according to visualization of
power Doppler in the quadrants
PI and PSV of vessels in
endometrium and
subendometrial area (<5mm)
Presence of endometrial and
subendometrial blood ow
; ≥5mm
2
USS
day Results
PSV between pregnant and nonpregnant cycles
Absent subendometrial ow associated
with no pregnancy
than non-pregnant cycles
Absent subendometrial ow associated
with no pregnancy
pregnancy rates in patients without
endometrial /subendometrial ow
times to become pregnant than those
with absent ow
USS
day Results
OR Higher EDPA in pregnant cycles
Lower implantation and
pregnancy rates when EDPA
2
<5mm
No difference in any USS
parameters between pregnant and
and
non-pregnant cycles
ET
hCG Implantation and pregnancy rates
similar in all grades of
endometrial vascularity
OR No difference in spiral artery PI
and PSV between pregnant and
non-pregnant cycles
Non-detectable spiral blood ow
was not associated with a lower
implantation rate
ET Absent endometrial and
subendometrial ow associated
with a lower pregnancy rate
E. H. Y. Ng
The presence of endometrial and subendometrial blood ow can be identied easily in 2D
Doppler ultrasound. Absent endometrial and subendometrial blood ow has been shown to be
associated with no pregnancy [15, 17] or a signicantly lower pregnancy rate [21, 22].
Endometrial andSubendometrial
Blood Flow by 3D Doppler
3D power Doppler ultrasound with the aid of the
VOCAL® (virtual organ computer-aided analysis) imaging program for the 3D power Doppler
3 Two-Dimensional andThree-Dimensional Doppler inReproductive Medicine
47
histogram has been used to measure endometrial
volume and indices of blood ow within the
endometrium (Fig. 3.2). Vascularization index
(VI), which measures the ratio of the number of
colour voxels to the number of all the voxels, is
thought to represent the presence of blood vessels
(vascularity) in the endometrium, and this was
expressed as a percentage (%) of the endometrial
volume. Flow index (FI), the mean power
Doppler signal intensity inside the endometrium,
is thought to express the average intensity of
ow. Vascularization ow index (VFI) is a combination of vascularity and ow intensity [23].
The subendometrium can be examined
through the application of ‘shell-imaging’ which
allows the user to generate a variable contour that
parallels the originally dened surface contour.
The VI, FI and VFI of the subendometrial region
are obtained accordingly (Fig. 3.3). The intraobserver and interobserver reliability of endometrial and subendometrial blood ow by 3D power
Doppler have been conrmed to be high with all
measurements obtaining an intra-class correlation of above 0.9 [24, 25].
Studies addressing the role of endometrial and
subendometrial blood ow measured by 3D
Doppler in IVF treatment are summarised in
Table3.3. Schild etal. [26] measured the subendometrial blood ow after pituitary downregulation but prior to ovarian stimulation and showed
that subendometrial VI, FI and VFI were signicantly lower in pregnant cycles than non- pregnant
ones. Logistic regression analysis found that the
subendometrial FI was the strongest predictive
factor for the pregnancy outcome among other
3D Doppler ow indices.
Kupesic etal. [18] performed 3D ultrasound
examination on the day of blastocyst transfer and
found that subendometrial FI was signicantly
higher in pregnant cycles. Subendometrial VI and
VFI were similar between pregnant and nonpregnant patients. Wu etal. [27] measured subendometrial blood ow on the day of hCG and
demonstrated that subendometrial VFI was signicantly higher in the pregnant group.
Subendometrial VI and FI were also similar
between pregnant and non-pregnant cycles.
Subendometrial VFI was superior to subendome-
trial VI, subendometrial FI and endometrial volume in predicting the successful outcome in the
receiver operating characteristics (ROC) curve
analysis.
On the day of oocyte retrieval, Dorn etal. [28]
compared the subendometrial blood ow before
and after an intravenous administration of
Levovist, which is a contrast agent and consists
of 99.9% of D-galactose. All subendometrial 3D
Doppler ow indices after the administration of
the contrast agent were signicantly higher than
those without the contrast agent. However, all
subendometrial 3D Doppler ow indices with
and without the contrast agent were comparable
between pregnant and non-pregnant cycles. The
results of this study suggested that the use of 3D
power Doppler ultrasound under a contrast agent
during IVF treatment provided no additional
advantage over the conventional 3D power
Doppler ultrasound examination.
Järvelä etal. [29] determined endometrial and
subendometrial VI after gonadotrophin stimulation but before hCG administration and again the
day of oocyte retrieval. There were no differences
between the pregnant and non-pregnant groups in
endometrial and subendometrial VI on either day
examined. I have published the largest study
involving 451 transfer cycles [30]. Patients in the
pregnant group had signicantly lower uterine RI,
endometrial VI and VFI than those in the nonpregnant group. Endometrial thickness, endometrial volume, endometrial pattern, uterine PI,
endometrial FI and subendometrial VI, FI and VFI
were similar between the non-pregnant and pregnant groups. The number of embryos replaced and
endometrial VI were the only two predictive factors for pregnancy in a logistic multiple regression
analysis. ROC curve analysis revealed that the area
under the curve was around 0.5 for all ultrasound
parameters for endometrial receptivity.
Implantation and pregnancy rates were comparable for patients with and without endometrial
and subendometrial blood ow [30]. This nding
is contradictory to those obtained by 2D Doppler
ultrasound, which suggested that absent endometrial and subendometrial blood ows were associated with no pregnancy [15, 17] or much
reduced pregnancy rate [21, 22].