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19 Ultrasound andOvarian Hyperstimulation Syndrome
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Aug 7.;2011:1.
Ultrasound Guidance inEmbryo
Transfer
AlbertoRevelli, TomerTur-Kaspa,
andEdmondConno
20
Introduction
High-resolution, high-frequency transvaginal US
has become an integral part of infertility evaluation and follicular growth monitoring during controlled ovarian stimulation (COS), as well as the
method of choice to achieve an efcient and rapid
oocyte harvesting [1, 2].
Embryo transfer (ET) is a more difcult procedure to master than oocyte retrieval and more
profoundly affects IVF outcome. In fact, the type
of catheter [3], the operator’s experience [4], the
site of embryo discharge [5–8], the catheter tip
contamination with mucus or blood [9], the presence of uterine contractions, and the difculty to
pass through the cervix [10–12] have all been
regarded as factors potentially affecting IVF
results.
For several years, ET was performed inserting
the catheter into the cervix and blindly discharging the embryos approximately in the middle of
the uterine cavity (“clinical touch” ET (CTET)).
A. Revelli
Sant’Anna Hospital, University of Turin, Department
of Obstetrics and Gynecology, Turin, Italy
T. Tur-Kaspa (*)
Wesleyan University, Middletown, CT, USA
E. Conno
Feinberg School of Medicine, Northwestern
University, Chicago, IL, USA
While today US is routinely used for it, pre-IVF
evaluation of the uterine and cervical anatomy
was previously performed by using hysterosalpingography (HSG), magnetic resonance imaging (MRI), and/or computerized tomography
(CT) (Figs.20.1, 20.2, and 20.3). US availability
and ease of performance have made sonohysterography (HSN) (see Chap. 12) the preferred
and cost- effective visualization method of the
uterus prior to ET [13, 14]. The so-called mock
ET was sometimes performed some days in
advance in order to predict the conditions that
would have been found during ET, but its predictive accuracy resulted to be quite poor [15, 16];
pre-ET US measurement of the cervical uterine
depth could verify the mock transfer data but still
was a poor predictor of ET success (Fig.20.3).
Routine US use before, during, and post ET has
now largely eliminated the discordance between
mock ET and live ET [17].
In 1985, Strickler [18] was the rst to describe
the use of US to guide ET.Since then, US guidance has gradually been added to achieve an
atraumatic, controlled, quick, and anatomically
dened ET.Indeed US guidance allows for better
control of the cervical trajectory and the uterine
depth, as well as to more precisely dene the site
of embryo replacement. Transabdominal US
allows for the visualization of the catheter tip in
real time, and both transabdominal and transvaginal techniques allow physicians and patients to
see an echogenic spot inside the uterus immedi-
© 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_20
335
336
A. Revelli et al.
ately after embryo discharge, giving a rather precise esteem of embryo position after ET.
Several prospective, randomized controlled
trials (RCTs) and meta-analyses have been performed to compare CTET to US-guided ET and
concluded that US guidance signicantly
increases the rate of easy transfers, ultimately
improving the clinical pregnancy rate and the
chance of a live birth [19–25].
This chapter will review the data available
today on the important role of US in ET.
Fig. 20.1 Pre-ET vaginal measurement of cervical-
fundal distance allows to calculate the site of embryo
discharge
Fig. 20.2 The mock transfer catheter is placed reaching
the site of embryo discharge
Fig. 20.3 A hyper-echogenic spot (bubble) after embryo
discharge indicates the place where the embryo has been
transferred
Clinical Touch ET Versus Transabdominal US-Guided ET
Several RCTs and systematic reviews compared the results obtained using the “blind”
clinical touch embryo transfer (CTET) technique with those of the transabdominal
US-guided transfer [19–25]. The main outcomes, being implantation rate, clinical pregnancy rate, and live birth rate, of IVF after
clinical touch ET were compared to those after
US-guided ET. In addition, other parameters
were investigated: miscarriage rate, multiple
and ectopic pregnancy rate, rate of difcult or
failed transfers, need for instrumental assistance during ET (e.g., stylette, tenaculum, dilatation), signs of cervical or endometrial trauma
(e.g., presence of blood, mucus, or both on the
catheter tip), and percentage of retained
embryos. Most RCTs and meta-analysis concluded that US guidance improves the chances
of clinical pregnancy and live birth compared
to the clinical touch method [19–25].
The presence of blood on the catheter tip that
is associated with decreased implantation, clinical pregnancy, and live birth rates, when compared to no blood, appeared to be less frequent
when performing ET under US guidance, as it
was much easier to avoid unwillingly touching
the fundus of the uterine cavity [26].
Furthermore, allowing visualization of the cervical canal, US guidance reduced unrecognized
events such as 180° curling of the inner catheter
and cervical deposition of the embryos, the need
20 Ultrasound Guidance inEmbryo Transfer
337
for instrumental assistance, and the failure to
transfer with the assigned catheter. US guidance
makes the ET procedure easier to perform, thus
it signicantly decreases the rate of diffuclt
transfers [27]. Differently, adding US guidance
had no signicant effect on nding mucus on
the catheter tip, on the percentage of transfer
with retained embryos, and on the rate of multiple pregnancy, ectopic pregnancy, and spontaneous miscarriage [19–25].
There are at least two mechanisms by which
US-guided ET may improve ART outcome: the
full bladder needed for transabdominal US
straightens the angle between the cervix and
the uterus, and by conrming the position of
the catheter tip, the embryo is discharged close
to the desired site. The optimal area of embryo
deposition in the uterine cavity, resulting in
higher PR, has been demonstrated to be
between 1.0 and 1.5cm from the fundus of the
cavity [7–9].
US guidance may also allow physicians to
perform, in the infrequent occasion when catheter access into the uterus is impossible, a transmyometrial ET (Fig. 20.4) which is performed
under conscious sedation using a coaxial needle
outtted with a matching ET catheter [28, 29];
this technique abolishes the need of an unplanned
laparoscopic intratubal ET.
The use of transabdominal US during ET
also has some disadvantages vs. CTET: (1) US
equipment and a second operator (physician,
nurse, or a technician) with adequate training in
transabdominal US are needed, increasing the
overall cost; (2) visualization of the catheter tip
might be suboptimal in overweight patients or
in a patient with a retroverted uterus—moving
the catheter back and forth inside the uterus
may be needed to better identify its position,
but this may potentially damage the endometrium; (3) the time needed to perform ET is longer with US guidance than with CTET; (4) the
patient must keep a full bladder for some time,
and this may cause discomfort and cramping,
possibly severe if a delay occurs for any reason;
and (5) the patient’s discomfort, in turn, may
stimulate uterine contractions. Moreover, some
physicians prefer CTET to minimize the need
to observe the cervix and the US screen
simultaneously.
Transvaginal Versus
Transabdominal US Guidance forET
The use of transvaginal US to guide ET (TVET)
was proposed claiming that it could be preferable vs. transabdominal-guided ET in some
patients (overweight or with uterine retroversion), more tolerable (no need of a full bladder), and more convenient (single operator
needed) [30, 31]. Indeed, TVET could potentially have some advantages. It does not require
a full bladder, allows an optimal detection of
the utero-cervical angle even in case of uterine
retroversion or overweight patients, and can
visualize the catheter tip better than transabdominal US. On the other side, however, it
might be difcult for the physician since it
requires manual skills to be performed simultaneously by a single operator and can be uncomfortable for the patient because of the necessity
to insert the US vaginal probe into the vagina
while the speculum is still in place. Then the
outer part of the transfer catheter will be
inserted into the cervix, and the speculum will
be removed while maintaining the probe in the
vagina. The nal step is inserting the softer
part of the catheter, loaded with the embryo(s),
and performing the ET under TVUS.
A couple of retrospective studies reported signicantly better IVF outcome using TVET vs.
CTET [32, 33], and two RCTs comparing TVET
vs. transabdominal-guided ET reported comparable clinical pregnancy and implantation rates
[34, 35] but were underpowered to reach convincing conclusions. While the duration of the
procedure was observed to be signicantly longer with TVET, it was associated with increased
patient comfort due to the absence of bladder
distension.
A simpler variant of TVET was recently proposed: transvaginal US is used just before ET in
order to measure the uterine length and calcu-
338
Fig. 20.4 Vaginal
US-guided
transmyometrial needle
placement in a partially
fused bicornuate uterus
(upper gure right).
Bubble markers are
present in both right and
left uterine horns
depicting proper
bilateral placement of
one embryo in each
uterine cavity (lower
gure)
A. Revelli et al.
late the optimal site for embryo discharge; then,
a clinical touch ET is performed, guiding the
embryo-loading cannula to the previously
calculated discharge site [36–39]. The uterine
length measurement followed by CTET was
already reported to obtain the same IVF outcome as transabdominal-guided ET in a retrospective study using historical controls [36].
The equivalence of the two methods was also
observed in a small RCT [37], whereas another
larger randomized trial (200 patients) showed
slightly higher implantation and pregnancy rates
in the group receiving CTET with previous uterine length measurement [38]. The largest RCT
[39], that was designed as a non-inferiority trial
and adequately powered to detect a clinically
relevant difference in IVF outcome, demonstrated that using uterine length measurement
20 Ultrasound Guidance inEmbryo Transfer
339
followed by CTET resulted in a similar implantation rate and clinical and ongoing pregnancy
rates compared to transabdominal-guided
ET. Moreover, the former technique was less
time-demanding, more easily performed by a
single operator, and standardized between physicians with different manual skills.
Training inEmbryo Transfer
US guidance may be successfully applied to
teach the transfer technique to young doctors
without compromising IVF outcome; it prevents
an involuntary touch of the uterine cavity fundus, potentially able to elicit myometrial contractility and reduce the likelihood of embryo
implantation.
The post-ET marker bubbles visualized on
US verify mid-cavity embryo placement
(Fig.20.5) and allow the physician, patient, and
spouse to observe the position of the embryo
placement. Although it is likely that embryos
move inside the uterine cavity according to
uxes in uterine uids [40, 41], visualizing
marker bubbles on the screens just after ET may
be reassuring about a correct embryo discharge.
Shah etal. [42] recently demonstrated that the
most important factor in learning a correct ET
technique obtaining high ET success rates was
the actual performing of live ETs rather than
practicing US-guided intrauterine inseminations. Also, the clinical experience of the ultrasonographer assisting US-guided ET was
observed to have no effect on the clinical outcome [43].
Coaxial catheter US-guided ET approach
involves initial placement of an outer catheter
in the internal uterine os (Fig.20.6). The outer
catheter protects the inner catheter from
mucus exposure and eliminates the need to
renegotiate a deviated or a branching cervical
canal. In this instance, time is not a limiting
factor because the embryos are loaded into
the inner catheter, while the outer catheter is
already in place. US will then allow ET time
to be less than 30s (Fig.20.7). US guidance is
extremely instructive at training facilities as it
can provide feedback and reassurance to physicians in training. Coaxial live ultrasoundguided ET allows for the teaching of ET
without a decline in PR.
Fig. 20.5 Abdominal
US with full bladder
depicts two marker
bubbles visualized in
mid-uterine cavity and
conrming a perfect
placement of embryos
340
Fig. 20.6 Abdominal
US depicts the external
coaxial catheter wedged
into the endometrium in
an anteverted uterus
(lower gure). Sliding a
rehearsal inner catheter
allows proper placement
in the lower uterine
segment (upper gure)
A. Revelli et al.
The American Society for Reproductive
Medicine (ASRM) published in 2017 a practice
guideline for performing ET, as well as a standard ET protocol template [3, 44]. Based on
evidence- based medicine, the ASRM recommends the following steps to improve pregnancy
rates: the use of abdominal US guidance for ET,
the removal of cervical mucus, the use of a soft
catheter for ET, and placing the embryo inside
the uterine cavity at least over 1.0cm from the
fundus. In addition, immediate ambulation following ET is also recommended [3, 44]. The
ASRM was actively involved in developing an
ET simulator which has been shown to improve
pregnancy rates and to decrease time to prociency in training REI fellows [45].
20 Ultrasound Guidance inEmbryo Transfer
Fig. 20.7 Abdominal
US demonstrates that
the outer coaxial
catheter is withdrawn
leaving the inner soft
embryo loaded catheter
at 1cm from the uterine
fundus (lower gure).
Under live US
observation, the embryo
is injected, and the
marker bubble is
observed in mid-cavity
(upper gure)
341
Conclusion
Recommendations to get an optimal ET, based on
expert opinions, include the performance of a
meticulous cervical mucus removal, mid-uterine
cavity embryo placement, a slow catheter withdrawal to avoid embryo dragging to the cervix,
and a short embryo load to unload time [46–48].
In addition, evidence-based guidelines encourage
US guidance in ET as it will result in easier ETs
and improved IVF outcome.
US has become an indispensable tool to guide
and verify proper embryo deposition in the
uterus. Importantly, patients take great comfort in
having the ability to visualize on the screen the
nal step of a difcult process.
The use of US guidance is now an integral part
of an ET worldwide. With the improvement in
342
A. Revelli et al.
imaging and the possibility of utilizing 3D and
4D US [49], ultrasound guidance may assist in
maximizing the potential for embryo implantation after ET and thus will further improve ART
outcome [3].
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