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Chapter 28: US-guided embryo transfer
48. Kojima K, Nomiyama M,
Kumamoto T, Matsumoto Y,
Iwasaka T. Transvaginal
ultrasound-guided embryo
transfer improves pregnancy
and implantation rates after
IVF. Hum Reprod 2001;
16(12): 2578–82.
49. Coroleu B, Barri PN,
Carreras O, et al. Effect of
using an echogenic catheter
for ultrasound-guided
embryo transfer in an IVF
programme: a prospective,
randomized, controlled
study. Hum Reprod 2006;
21(7): 1809–15.
50. Karande V, Hazlett D,
Vietzke M, Gleicher N.
A prospective randomized
comparison of the Wallace
catheter and the Cook EchoTip catheter for ultrasoundguided embryo transfer.
Fertil Steril 2002; 77(4):
826–30.
51. Wood EG, Batzer FR, Go KJ,
Gutmann JN, Corson SL.
Ultrasound-guided soft
catheter embryo transfers
will improve pregnancy
rates in in-vitro fertilization.
Hum Reprod 2000; 15(1):
107–12
52. Allahbadia GN, Athavale
UR, Kadam KS, Gandhi GN,
Digra GS, Kaur K. A
prospective randomized
comparison of the Wallace
catheter and the SureView
catheter for ultrasoundguided embryo transfer
(ET). Fertil Steril 2005;
84(1): S117.
53. Aboulfotouh I, Abou-Setta
AM, Khattab S, Mohsen IA,
Askalani A, el-Din RE.
Firm versus soft embryo
transfer catheters under
ultrasound guidance: does
catheter choice really
influence the pregnancy
rates? Fertil Steril 2008;
89(5): 1261–2.
54. Letterie GS. Threedimensional ultrasoundguided embryo transfer: a
preliminary study. Am J
Obstet Gynecol 2005;
192(6): 1983–7.
55. Gergely RZ, DeUgarte CM,
Danzer H, Surrey M, Hill D,
DeCherney AH. Three
dimensional/four
dimensional ultrasoundguided embryo transfer using
the maximal implantation
potential point. Fertil Steril
2005; 84(2): 500–3.
56. Edwards RG, Fishel SB,
Cohen J, et al. Factors
in
fluencing
in vitro
alleviating human infertility.
J In Vitro Fert Embryo Transf
1984; 1:3–23.
the success of
fertilization for
233
Chapter
Ultrasonography-guided embryo transfer:
29
clinical experience
Mostafa Abuzeid and Botros Rizk
Introduction
Successful outcome after in-vitro fertilization-embryo transfer
(IVF-ET) depends on embryo quality, endometrial receptivity,
and the technique of embryo transfer. Meticulous and atraumatic transfer procedure is essential for successful outcome
[1,2,3,4]. Rizk (2008) noted a strong correlation between the
ease of embryo transfer and the pregnancy rate [4,5,6,7,8,9].
Unfortunately, there is a reluctance to adopt new techniques of
embryo transfer (ET) among clinicians [8]. In addition, there is
little attention in the literature to this procedure compared with
other steps of in-vitro fertilization treatment [3]. In this chapter
we briefly review the principles for optimizing chances
of successful ET and the role of ultrasound scan in ET. There
will be emphasis on some practical points regarding ET
techniques.
Effect of cervical mucus and blood
The presence of cervical mucus has been thought to increase
rates of embryo retention and embryo expulsion [10]. It may
also be a source of embryo contamination [11,12]. In addition,
it may be present in the endometrial cavity as an extension from
the cervical canal (Figure 29.1).
Furthermore, fluid may inadvertently enter the endometrial
cavity during cervical lavage prior to ET [13,14]. Every effort
should be made to carefully remove cervical mucus prior to ET.
This requires gentle and through technique of suction and
gentle irrigation using flushing media. The mere presence of
blood is suggestive of difficult transfe r. The presence of blood is
associated with poor pregnancy rate due to difficult transfer rate
and its sequelae and also due to the increased chance of embryo
retention [8].
Uterine contraction
Uterocervical contraction could lead to embryo expulsion. One
should therefore strive to avoid initiation of uterine contractions during ET. Stimulation of the cervix by grasping of the
cervix with a tenaculum can cause uterine contractions through
release of oxytocin [15]. In addition, passage of the outer rigid
sheath of the ET catheter through the internal os may lead to
(a)
Figure 29.1. (a) Transvaginal ultrasound scan illustrating fluid in the endometrial cavity as the result of cervical mucus reaching into the lower area of the endometrial
cavity. (b) Transvaginal ultrasound scan illustrating no fluid in the endometrial cavity after cervical mucus has been aspirated.
Ultrasonography in Reproductive Medicine and Infertility, ed. Botros R. M. B. Rizk. Published by Cambridge University Press. © Cambridge
University Press 2010.
(b)
Chapter 29: US-guided embryo transfer
prostaglandin release. Furthermore , touching the uterine
fundus, especially with a rigid catheter, can initiate uterine
contractions [16].
Proper delivery of embryos inside the uterine cavity
Meticulous ET should ensure proper delivery of embryos inside
the uterine cavity (Figure 29.2). This depends on several factors,
including uterocervical angle, length of cervical canal, and how
far the ET catheter is advanced. The so-called problematic
cervix that leads to difficult ET procedure and perhaps inadequate transfer of embryos into the uterine cavity is most
commonly secondary to distortion in the cervical canal or
uterocervical angle. Figure 29.3 illustrates different types of
uterocervical angles [17].
Figure 29.4 depicts transvaginal ultrasound pictures of dif-
ficult uterocervical angles that may complicate ET procedures.
Such distortions are usually congenital in nature, sometimes as
(a)
a result of cervical fibroid (Figure 29.5) and/or rarely as a result
of a large nabothian follicle (Figure 29.6), or multiple nabothian
follicles (Figure 29.7).
In our experience, we rarely come across a true cervical
stenosis, although theoretically this could be present as a result
of previous surgery on the cervix, e.g., cone biopsy. Cervical
polyp may also interfere with ET procedure and should be
removed prior to IVF-ET.
An unusual angle can be seen in patients with acutely anteverted/anteflexed uterus or with retroverted uterus, especially if
it is retroverted and fixed secondary to pelvic adhesions. It is
also found in patients with extensive pelvic adhesions, leading
to tilting of the uterus to one side, i.e., laterally. The uterus
may also be tilted to one side – leading to an unusual lateral
angulation in patients with unicornuate uterus – especially
in association with endometriosis and pelvic adhesions .
In rare cases, the uterocervical angle may have the shape of
almost a half-circle appearance for no obvious reason
(Figure 29.8).
(b)
(c)
Figure 29.2 (a–d). Transvaginal ultrasound scans illustrating proper advancement of the ET catheter into the endometrial cavity to ensure correct delivery of embryos
inside the endometrial cavity.
(d)
235
Section 3: Ultrasonography in assisted reproduction
(a)
(c)
(b)
(d)
Figure 29.3. Transvaginal ultrasound scan of uterocervical angle. (a) No angle; (b) small angle (<30°); (c) moderate angle (30–60°); (d) large angle (>60°).
(a)
Figure 29.4 (a, b). Transvaginal ultrasound scan of difficult uterocervical angles: almost 90°.
Sometimes the difficulty is due to a narrowed external os,
when it is difficult to advance the outer catheter. Sometimes the
cervix is very short, and flush with the lateral fornix.
Some patients who underwent cesarean section may have
an acute angle between the cervical canal and the lower
uterine segment. This may be secondary to a healed cesarean
scar pulling on and distorting this area. Others may occasionally have a distorted angle as a result of adhesions
between the uterus and the anterior abdominal wall. In
addition, the cervix may also be high in position after
(b)
236
Chapter 29: US-guided embryo transfer
Table 29.1. Principles that optimize the chances of successful ET
Proper evaluation of the uterine cavity and cervical canal
Thorough and gentle removal of cervical mucus and avoidance of cervical
bleeding
Avoidance of initiation of uterine contractions
Proper delivery of the embryos inside the uterine cavity
Figure 29.5. Cervical fibroid distorting uterocervical angle.
(a)
(b)
cesarean section, which can make it difficult to visualize the
cervix.
Optimizing embryo transfer procedure
Certain steps need to be adopted to optimize ET procedure and, in
turn, the chances of pregnancy (Table 29.1). Most of these steps are
done on the day of ET, but some of them should be done well ahead
of the ET procedure, i.e., prior to starting ovulation induction and
certainly prior to retrieval procedure. Certain pathologies that may
influence treatment or interfere with implantation or with ET
procedures need to be identified and dealt with. History, physical
examination, transvaginal ultrasound scan, saline sonogram, and
mock ET trial are mandatory steps. The use of 3D ultrasound to
detect subtle abnormalities, especially arcuate uterus and short
uterine septum, is gaining momentum. Table 29.2 illustrates ovarian, fallopian tube, cervical, uterine, and endometrial cavity issues
that need evaluation. Any significant pathology, e.g., submucous
fibroid (Figure 29.9), or uterine septum (Figures 29.10, 29.11,
29.12, 29.13, 29.14), needs to be corrected surgically prior to IVF
treatment.
When a problematic cervix is identified, a plan of action needs
to be formulated. Currently most practitioners performET under
ultrasound guidance. This helps in making the ET procedure easy
and atraumatic and, in turn, optimizes the chances of a successful
transfer. In some patients the problem can be solved by bladder
distension and ultrasound guidance. In others, a cervical suture
needs to be placed on the day of retrieval, to be used for traction
and straightening of the uterocervical angle.
Figure 29.15 illustrates an ET catheter tip in a false passage.
In some patients, modified general anesthesia may be needed,
(c)
Figure 29.6. (a, b) Large nabothian follicle near the region of the internal os.
(c) A large nabothian follicle near the region of the internal os interfering with
advancement of the ET catheter tip into the endometrial cavity.
and in others transvaginal ultrasound-guided ET may
be required. In a few patients, cervical dilatation and even
hysteroscopy and resection of a ridge may be required [18,19].
In this case, some investigators suggest leaving a Foley catheter
237
Section 3: Ultrasonography in assisted reproduction
Table 29.2. Transvaginal gynecologic ultrasound evaluation prior to IVF-ET
treatment
1. Ovary Position of ovary – accessible or not
PCO changes
Ovarian cysts, e.g., endometriomas
Dermoids
2. Fallopian
tube
3. Cervical
canal
4. Uterus Size
Hydrosalpinx
Large paratubal cyst
Length
Nabothian follicles
Polyps
Fibroids
Fibroid tissue
Curve
Assessment of utero cervical angle
Position Anteverted
Retroverted
Axial
Lateral tilt (2° to
adhesions)
Adhesions to abdominal wall, e.g., after cesarean section
Fibroids
Adenomyosis
Distortion of endometrial
cavity
Type of endometrial lining
Effect of previous cesarean section
Polyps
Submucous fibroids
Adenomyosis
Scar tissue
in utero for one week after such procedures [19]. If a mock trial
is impossible and in the presence of at least one patent and
healthy fallopian tube, tubal transfer, e.g., gamete intrafallopian
transfer or tubal embryo transfer, should be planned
(Figure 29.16).
On the day of oocyte retrieval, transvaginal ultrasound
evaluation for a variety of issues should be performed, as
summarized in Table 29.3.
On the day of ET, transabdominal ultrasound scan-guided
ET should be planned. Table 29.4 summarizes some important
points during this procedure. At the time of ET, bladder filling
should be optimum (Figures 29.17, 29.18, 29.19). It should not
be underdistended or overdistended (Figure 29.20).
Figure 29.21a illustrates fluid in the endometrial cavity, while
Figure 29.21b illustrates the endometrial cavity after fluid has
been aspirated before the ET procedure. Table 29.5 summarizes
some important practical points that need to be adopted to
optimize ET procedure. Patients who have undergone cesarean
section require adequate evaluation to determine whether they
have some of the factors that may make the ET procedure
difficult. In some instances, the uterus may be adherent to the
anterior abdominal wall (Figure 29.22) and, in turn, the cervix
may be high in position.
In these cases, one cannot use a short catheter (18mm). A
suture on the anterior lip of the cervix on the day of retrieval
may be helpful. In addition, the bladde r should not be very full
as it will never be in front of the uterus and it may potentially
create a curve between the cervical canal and endometrial cavity
(Figure 29.23). In some patients the C-section scar in the lower
uterine segment may lead to an unfavorable angle between the
cervix and the endometrial cavity (Figure 29.24).
In turn, a false passage can be created as one is passing the
catheter through the cervical canal. Application of cervical
traction by pulling on a suture placed in the anterior lip of the
cervix may help in straightening that angle, reduce the likelihood of false passage, and facilitate the process of ET [20].
Alternatively, advancing the outer sheath more than usual after
fashioning its curve may help in overcoming the problem.
When it is impossible to perform a mock trial, it is better to
consider tubal embryo transfer (TET) [21] or gamete intrafallopian transfer (GIFT) [22], providing one fallopian tube is
patent and healthy (Figure 29.16). Otherwise, if both tubes are
damaged, one may utilize the technique of transmyometrial
surgical ET proposed by Kato et al. [23].
Embryo transfer under ultrasound guidance
Woolcott and Stanger have demonstrated suboptimal placement of the catheter tip in approximately 50% of patients
when transvaginal ultrasound-guided ET was performed [24].
In fact, they showed subendometrial placement of the tip of the
catheter in 24.8% (Figures 29.25, 29.26); the catheter tip was
abutting the fundus in 17.4% and near the opening of the
fallopian tube in 7.4% [24]. Strickler et al. [25] were the first
to use transvaginal ultrasound to ensure proper positioning of
the ET catheter. The technique has been adopted by several
investigators [26,27,28,29].
Transabdominal ultrasound-guided ET has been shown not
only to improve the ease with which the procedure of ET is
done [30], but also to imp rove the pregnancy rate [31] and
delivery rate [32]. This is logical because, during ultrasoundguided ET, one can see the tip of the catheter as it advances
through the cervical canal. One is able to determine how far the
tip of the catheter has advanced into the endometrial cavity
(Figure 29.27) and one can ensure that the catheter is along the
endometrial cavity and not in a false passage.
One of the challenges is the relationship between the
cervical canal and the endometrial cavity. In some cases,
owing to retroversion and less commonly to acute anteversion,
there may be a bad angle that makes it difficult to negotiate the
cavity. This angle can also be due to a curved cervical canal.
Sometimes there is a curve in the endometrial cavity, giving it a
banana shape (Figure 29.28). This could be secondary to
238
Chapter 29: US-guided embryo transfer
(a)
Figure 29.7. (a) Multiple nabothian follicles in the cervical canal. (b) Multiple nabothian follicles not interfering with mock trial.
(b)
Figure 29.8. Uterocervical angle having the shape of almost a half-circle in
appearance.
Figure 29.9. 3D saline sonogram illustrating type 2 fundal submucous fibroid.
Figure 29.10. 3D ultrasound illustrating a short, incomplete uterine septum.
Figure 29.11. 3D ultrasound illustrating a long, complete uterine septum.
239
Section 3: Ultrasonography in assisted reproduction
Table 29.3. Transvaginal gynecologic ultrasound evaluation on day of oocyte
retrieval
Size of ovaries
Number of follicles
Position of ovaries
Aspiration of hydrosalpinx
Aspiration of cervical mucus
Aspiration of endometrial fluid
Aspiration of a large cervical cyst
Fluid in peritoneal cavity
Table 29.4. Transabdominal gynecologic ultrasound scan on day of ET
Bladder size should be optimal Not overdistended
Not underdistended
Aspirate cervical canal under direct vision
Trial catheter under direct vision
Transfer catheter only when situation under control
Transfer catheter in complete view all the time
Figure 29.12. 3D ultrasound illustrating asymmetric cornual regions as a result
of the short, incomplete uterine septum with its apex deviated to one side.
Figure 29.13. 3D ultrasound illustrating asymmetric cornual regions as a result
of the short, incomplete uterine septum with its apex deviated to one side.
adenomyosis in the posterior wall of the myometrium, or to an
intramural fibroid.
Ultrasound guidance allows the clinician to visualize the tip
of the catheter as it is advanced along the cervical canal into
the endometrial cavity (Figure 29.27). It therefore confirms that
the catheter is advanced beyond an angle along the course of the
cervical canal instead of the tip going into a false passage. In
Figure 29.14. 3D saline sonogram illustrating a long, complete uterine septum.
Figure 29.15. Transvaginal ultrasound scan of a retroverted uterus with
embryo transfer catheter tip in a false passage in the myometrium.
addition, it ensures that the tip of the catheter is beyond the
internal os in cases of elongated cervix and, thus, avoids transfer
of embryos into the cervical canal. Furthermore, ultrasound
guidance facilitates placement of soft catheters; it avoids touching the anterior or posterior fundus walls; and it allows the
direction the catheter along the course of the endometrial
cavity, in turn avoiding shearing of the endometrium causing
bleeding, or plugging of the catheter tip, which may lead to
retention of the embryos. It enables the clinician to deposit the
embryos in the desired area near the uterine fundus and, more
importantly, the clinician is able to visualize the ease with which
240
Chapter 29: US-guided embryo transfer
Table 29.5. Practical points that optimize the ET procedure
Medication Motrin
Valium
Sedation
Size of speculum
Position of speculum
Lateral retractor
Suture in the: Anterior lip
Posterior lip
Type of catheter: Soft catheter
Echogenic catheter
Stylet catheter
Curve of catheter
Need to advance rigid outer sheath through internal os
(a)
(b)
Figure 29.16. Illustrating a technique of tubal embryo transfer.
Figure 29.17. Perfect bladder distension.
(c)
Figure 29.18 (a–c). Perfect bladder distension, which allows clear view of
endometrial lining and, in turn, perfect advancement of ET catheter along the
endometrial cavity and proper delivery of embryos in the desired area.
241
Section 3: Ultrasonography in assisted reproduction
(a)
(b)
(c)
Figure 29.20. Overdistended bladder. Note: the endometrial lining is not clear.
(a)
(b)
242
Figure 29.19 (a–c). Perfect bladder distension, which allows clear view of
endometrial lining and, in turn, perfect advancement of ET catheter along the
endometrial cavity and proper delivery of embryos in the desired area.
Figure 29.21. (a) Fluid in the endometrial cavity. (b) Same patient after
aspiration of endometrial fluid using a Wallace embryo transfer catheter on the
day of oocyte retrieval.