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Chapter 6: Diagnostic hysteroscopy
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Sardo A, Taylor A,
63
Chapter
Ethics of ultrasonography
7
Ethics is the branch of science that deals with human morality – right and wrong behavior or virtues and vices. The
prime question that ethics addresses is “What ought our
behavior to be?” In medicine, ethics has been embodied in
the venerable Hippocratic Oath and aphorisms that have
provided a guide over the centuries to how physicians should
deal with their patients. Over centuries, medical ethics has
been influenced by traditions, attitudes, cultural and religious
beliefs, and social obligations. Indeed, issues of civil and
women’s rights added to concepts of individual autonomy
and outlined principal lines that should be considered within
the context of ethics.
Because the implementation of innovative medical technologies can raise unprecedented ethical, legal and social dilemmas, ethics is nowadays an emerging subdiscipline in
ultrasound practice as several clinical situations can only be
identified and addressed by ethical appreciation. This is particularly so in the area of antenatal screening, which is dominated
by the language of risk and probabilities. By their definitions,
obstetrics and gynecology are the branches of medicine that
touch most closely maternity and the privacy of the family.
Among all civilizations and cultures, dealing with women has
its own particular form and codes. In some ancient cultures,
women are gods in temples and their lives are taboos surrounded with secrets.
Ethics has two main principles: beneficence and autonomy
of the patient; in other words, the best interests of the patient
and her or his right to choose.
Osama M. Azmy and Kareem El-Nahhas
The principle of beneficence
The physician should serve the best interests of the patient.
This can be considered from different perspectives; one is the
doctor’s perspective whereby, based on scientificknowledge,
shared clinical experience, and rigorous clinical judgme nt,
the doctor can identify and serve what is best for his or her
patient [1]. The other perspective acknowledges that the
health-related interests of patients are a function of the
competencies of medicine as a social institution rather than
a function of the personal or subjective outlook of the
physician [2].
The principle of autonomy
The principle of autonomy recognizes that it is the voluntary
decision of the patient to authorize or refuse clinical management based on adequate and complete disclosure by the
physician about the patient’ s condition and management with
the understanding of this information by the patient [3]. This is
the basis of the concept of informed consent.
In the area of obstetric ultrasound, these rights are complete
and integral, but they may conflict with one another [4]
because, on the one hand, the mother and child are independent
beings and are incommensurable bearers of these rights. But at
the same time the pregnant woman and her unborn child are
interconnected in such a way that what benefits one may harm
the other.
There are obviously beneficence-based and autonomybased obligations to the pregnant woman during ultrasound
examination. Although the unborn child does not possess any
legal rights, in terms of autonomy or beneficence, it is expected
that each mother will by nature look after the best interests of
her unborn child [5].
Women’s autonomy
Indeed, ultrasound examination is considered by women a safe
procedure that causes no physical damage. They consider
it “intervention” only when the transducer is introduced
through an orifice such as the vagina. Although concerns have
been raised about pregnant women viewing ultrasound scans as
benign, many of the women reported having thought carefully
through their own moral beliefs and values prior to screening
[6]. Furthermore, the American College of Obstetricians and
Gynecologists has endorsed the “Prudent Use” statement from
the American Institute of Ultrasound in Medicine based on
ethical purposes discouraging the use of obstetric ultrasonography for nonmedical reasons, e.g., solely to create keepsake
photographs or videos [7]. Thus, ultrasound examination
requires the woman’s consent as this examination collects
information about her physical condition. When the examination is indicated and is done solely for the health of the woman,
consent is easily secured. Generally this indication exists if the
Ultrasonography in Reproductive Medicine and Infertility, ed. Botros R. M. B. Rizk. Published by Cambridge University Press. © Cambridge
University Press 2010.
Chapter 7: Ethics of ultrasonography
examination is expected to produce a result that has therapeutic
implications (even if it is the absence of a condition [8] that
would have therapeutic implications, i.e., no treatment is
required). One study [9] has emphasized that women’s understanding of ultrasound does not meet the requirements of
informed choice. This cross-sectional study evaluated women’s
understanding of prenatal ultrasound and was conducted to
evaluate how information is provided, women’s perceived
value of the information received, and their understanding of
ultrasound in relation to the principles of informed choice. One
hundred and thirteen women completed a questionnaire prior
to their 18-week ultrasound scan. Fifty-five percent stated they
received no information from their care provider. Only 31.9%
considered health care providers as a “very helpful” source of
information. Yet 69.0% stated that their care provider gave
them information that facilitated their understanding.
Specifically, 46.0% did not view ultrasound as a screen for
anomalies; some were uncertain about the safety (18.6%), diagnostic capabilities (26.5%), and limitations of testing (37.2%).
If the woman refuses the ultrasound examination, her wish
must be respected. The woman has the right to refuse without
giving any reason for her refusal. In this situation, the physician
has to counsel the patient of the possible consequences and
hazards that may affect her upon this refusal. If the patient
refuses the ultrasound examination due to the fears of its
harmful effects, the physician must clarify the facts to the
patient, support her, and illuminate her fears. During obstetric
ultrasound scanning and in occasional circumstances where the
unborn child may suffer from a condition that needs a treatment and this treatment threatens the mother’s life, there must
not be any obligation upon her to tolerate this treatment [10].
All fetal treatment necessitates accessing the fetus through the
pregnant woman’s body, and nonsurgical treatments have long
been a part of pregnancy care. However, recent developments in
this area, including the increasing routinization of sophisticated
antenatal ultrasound screening and the introduction of treatments including fetal surgery, may mark a shift in this specialty.
There are apparent effects of the orientation of fetal medicine
on prevalent conceptualizations of the maternal–fetal relationship, and some of the consequences of this. It is argued that new
forms of uncertainty, including complex risk and diagnostic
information, and uncertain prognostic predictions set within
the rhetoric of nondirective counseling and women’s choice, are
leading to unprecedented ethical issues within this area [11].
More widespread debate about such potential dilemmas needs
to take place before, rather than following, their introduction.
In other words, the pregnant woman has the right to accept or
refuse this treatment even if the treatment would be life-saving
for the unborn child. No such treatment is conceivable that
does not act on the child by going “through the mother” in
some way, inevitably invading the physical integrity of the
pregnant woman. So any treatment for the child requires consent from the mother and the pregnant woman is not held
responsible for the consequences of not treating her unborn
child [12].
The unborn child’s autonomy
Special situations are unique to obstetric ultrasound scanning,
where the physician is dealing with two living individuals at the
same time and where treati ng one may inevitably produce
harmful or untoward effects on the other.
The autonomy of the unborn child is an area of debate. The
silence that surrounded rigorous ethical debate served to highlight where discussion lay – namely, with the justifications
offered for the unborn child added to the dilemma of autonomy.
In the authors’ view and that of others [13], the fetus is a human
being that has all the appropriate rights from the date of conception. However, because we lack a method of communicating
with and understanding the unborn’s needs, and he or she does
not have the opportunity to express their own decisions, we
cannot uphold that right. Furthermore, the development of 4D
ultrasound technology has revolutionized fetal imagery by
offering direct visual access to realistic images of the fetus in
utero. These images, which claim to show a responsive being
capable of complex behavior, have renewed debate about the
personhood of the fetus [14]. The application of this statement
should not contradict with the woman’s right to choose. Others
believe that the fetus has autonomy only if viable and not as
such in the pre-vital state, and that only the woman can confer
such status on it [15]. Concerning the health aspects of the
unborn child, the responsibility may be on the mother, the
father, and/or the physician. However, this responsibility and
authority must be subordinate to the mother’s right of selfdetermination over her own body, because anything done to
the unborn child has to “go through” the mother. Thus, only the
mother can represent her unborn child when prenatal treatment
is required. The woman is free to act or not to act according to
her own values and beliefs. The responsibility of the managing
physician to the fetus in all cases should be balanced against the
obligations to the pregnant woman. Also, one should not ignore
that the ethical problems surrounding prenatal screening are
intensified in low-income settings [16], which points to the need
for research that takes into account the wider social context that
structures ethical dilemmas.
Key points in clinical practice
*
Always maintain professionalism. The patient must be
addressed by her preferred name. Never make remarks
relating to bodily appearance such as tattoos, piercing, or
suntan.
*
Be careful and explain to the patient what you are going to
do in the examination and provide ample information to the
patient about the purpose of the procedure.
*
Contain and respect the patient’s autonomy and the right to
refuse the procedure and do not begin it until she gives her
consent.
*
During examination, always maintain the patient’s
dignity. The patient should not be left undressed for
long. Use a gown or a sheet to cover her body during
65
Section 1: Imaging techniques
examination. Make sure that the examination room is
secured from unexpected intrusion.
*
Ensure the patient’s privacy, by providing comfortable and
pleasant conditions and adapt a comfort place in which the
patient can change in privacy.
*
Always obtain a chaperone. This chaperone is a source of
support, guidance, and help for the patient.
*
Give your patient your mind and your full attention. Let her
feel that the time of examination belongs exclusively to her
and respond to the patient’s questions and concerns. This
attitude will pay healthy dividends for both of you.
*
Maintain confidentiality of the acquired patient
information, and discuss the findings on the screen with
your patient.
Conclusion
Ethics as a subdiscipline of ultrasound examination and intervention has significant clinical implications. Failure to consider
these clinical implications of the ethical principles of beneficence and women’s autonomy is regarded as unacceptable and
unprofessional. Ultrasound societies should include training in
ethics, the use and misuse of ultrasound, and good technique
and understanding of implications for clinical care to improve
sensitivity. It is argued that innovative health technologies may
be changing the roles of both women and health practitioners,
and raising new issues, including ethical, legal, and social
dilemmas.
References
1. Cooper TR, Caplan WD,
Garcia-Prats JA, Brody BA.
The interrelationship of
ethical issues in the transition
from old paradigms to
new technologies. J Clin
Ethics 1996; 7(3):
243–50.
2. Gorincour G, Tassy S,
LeCoz P. The moving face of
the fetus-the changing face
of medicine. Ultrasound
Obstet Gynecol 2006; 28(7):
979–80.
3. Boyle RJ, de Crespigny L,
Savulescu J. An ethical
approach to giving couples
information about their
fetus. Hum Reprod 2003;
18(11): 2253–6.
4. Chervenak FA, McCullough
LB. Scientifically and ethically
responsible innovation and
research in ultrasound in
obstetrics and gynecology.
Ultrasound Obstet Gynecol
2006; 28(1): 1–4.
5. Strauss RP. Beyond easy
answers: Prenatal diagnosis
and counseling during
pregnancy. Cleft Palate
Craniofac J 2002; 39(2):
164–8.
6. Kongnyuy EJ, van den Broek
N. The use of ultrasonography
in obstetrics in developing
countries. Trop Doct 2007; 37
(2): 70–2.
7. ACOG Committee Opinion.
Non-medical use of obstetric
ultrasonography. Obstet
Gynecol 2004; 104(2): 423–4.
8. Chervenak FA, McCullough
LB. Ethics in fetal medicine.
Baillieres Best Pract Res Clin
Obstet Gynaecol 1999; 13(4):
491–502.
9. Williams C. Dilemmas in
fetal medicine: premature
application of technology
or responding to
women’s choice? Sociol
Health Illn 2006;
28(1): 1–20.
10. Kohut RJ, Dewey D, Love EJ.
Women
’s
knowledge of
prenatal ultrasound
informed choice. J Genet
Couns 2002; 11(4):
265–76.
11. McFadyen A, Gledhill J,
Whitlow B, Economides D.
First trimester ultrasound
screening. Carries ethical
and psychological
implications. BMJ 1998;
317(7160): 694–5.
12. Gagen WJ, Bishop JP. Ethics,
justification and the
prevention of spina bifida.
J Med Ethics 2007; 33(9):
501–7.
13. Savell K. Life and death
before birth: 4D ultrasound
and the shifting frontiers
of the abortion debate.
J Law Med 2007; 15(1):
103–16.
14. Greenland P, Lloyd-Jones D.
Critical lessons from the
ENHANCE trial. JAMA
2008; 299(8): 953–5.
15. Barnett SB. Live scanning at
ultrasound scientific
conferences and the need for
prudent policy. Ultrasound
Med Biol 2003; 29(8):
1071–6.
16. Gammeltoft T, Nguyen HT.
Fetal conditions and fatal
decisions: ethical dilemmas
in ultrasound screening
in Vietnam. Soc Sci
Med 2007; 64(11):
2248–59.
and
66
Section 2
Chapter
8
Ultrasonography in infertility
3D Ultrasonography and infertility
Jose M. Puente and Juan A. Garcia-Velasco
Introduction
Imaging in gynecology, and specifically gynecologic imaging as
it pertains to reproduction, refers almost exclusively to ultrasound imaging. In recent years, we have witnessed tremendous
advances in ultrasound (US) techniques such as 2D, 3D, and 4D
B-mode US. Reproductive medicine has also greatly benefited
from advances in pulsed, color, and power Doppler.
Three-dimensional US is a valuable new tool for the reproductive field. The ability to acquire and store ultrasonographic
volumes provides several advantages over preexisting techniques. First, we can load the volume in a computer for later
analysis: thus, the images can be evaluated after patient consultation and can easily be sent to a colleague for further analysis if
necessary. Second, 3D US is a great tool for teaching. The ability
to recreate a volume allows visualization of images in the three
orthogonal space sections and also allows generation of any
section in which the desired organ can be visualized perfectly;
this is something that can be difficult to achieve using 2D US.
Three-dimensional US also has some unique capabilities
that significantly enhance diagnosis. For example, it is quite
difficult to obtain a coronal sectio n using 2D US but very simple
using 3D US. This greatly facilitates accurate diagnosis and
characterization of uterine abnormalities, especially the difficult
differential diagnosis of a septate uterus versus a bicornuate
uterus. Through tomographic US imaging (TUI), a series of
extremely useful tomographic images are obtained which can
be used, for example, to visualize a uterine leiomyoma protruding toward the endometrial cavity (Figure 8.1). The
inverted mode of 3D US facilitates evaluation of antral follicles
(Figure 8.2). Organ volume can be calculated using the software
provided with the ultrasound equipment; the most widely used
is “virtual organ computer-aided analysis” or VOCAL. This
imaging program calculates organ volume from the areas of
the three orthogonal sections, allowing very precise calculation
of ovarian and endometrial volumes (Figure 8.3).
Combining power Doppler and 3D US allows the study of
tissue vascularization. First, the organ volume is obtained using
power Doppler. Subsequently, indexes such as the vascularization index (VI), the flow index (FI), and the vascularization-flow
index (VFI) are obtained by comparingthe number and intensity
of the colored voxels (similar to pixels in 2D US) with the gray
voxels. This technology has proved useful in the development of
endometrial receptivity markers and oocyte quality/quantity predictors based on endometrial/ovarian vascularization status.
Although results so far have been mixed, new studies will help
further refine this method There are some drawbacks to 3D US.
The equipment can pose technical difficulties – since the techniques involved are complex and there is a very wide spectrum of
possibleapplications, there is a longer learning curve for users. In
addition, different commercial machines and software lack compatibility, complicating or even preventing data interchange and
multicenter studies. Finally, delayed image-processing means
that 3D US involves extra work and thus extra time. There is
tremendous potential for the use of 3D US in two scenarios: for
use in basic research and in clinical studies, and for wider use in
all reproductive medicine units, so that clinicians who currently
routinely use 2D US can benefit from the advantages of this
newer technology.
Estimating the ovarian reserve with 3D US
Antral follicle count in both ovaries, preferentially performed
during the menstrual cycle or in the early follicular phase, is
currently considered the gold standard for estimating the ovarian
reserve. Follicle count can be evaluated by either 2D US or 3D
US [1], since both modalities have shown good inter- and intraobserver correlation. The antral follicle count results using 2D
and 3D US are generallyvery similar, although 3D US is superior
for estimates in ovarieswith a very high antralfolliclepopulation.
Some US machines display “inversion mode,” which provides an
inverted image, similar to the image in a photographic negative.
Using the inversion mode, visualizationoftheovarianparenchyma
is suppressed and follicles, which appear white, can be counted
more easily. Image or volume rotation, either manually or automatically using cine-loop, facilitatesthisprocess.Inversionmode
can be used to diagnose low responders and is easy to implement.
Currently, the greatest disadvantage of 3D US is the amount
of time required to perform it. It has been estimated that an
expert professional needs 20–30 minutes [2], and another additional 5–10 minutes are required if vascular flow is analyzed.
This reduces the chances of real-time decision-making and the
Ultrasonography in Reproductive Medicine and Infertility, ed. Botros R. M. B. Rizk. Published by Cambridge University Press. © Cambridge
University Press 2010.
Section 2: Ultrasonography in infertility
Figure 8.1. Hyperstimulated ovary. TUI mode allows obtaining millimetric images of the selected structure.
immediately calculates the volume and mean follicle diameter.
This method reduces human error due to measuring only two
sections, and also saves time and enables immediate discussion
with patients about changes in medication. This software may
improve follicle measurements, although studies are needed
before its widespread use is implemented (Figure 8.4).
Three-dimensional US is an excellent technique for calculating ovarian volume very precisely. Using the VOCAL program and observing the ovary with rotating angles between 9°
and 15°, the ovarian volume can easily be estimated with a
sagittal section. Low ovarian reserve and poor response to
controlled ovarian hyperstimulation in assisted reproductive
technology (ART) is associated with ovarian volumes <3 ml,
whereas polycystic ovaries are associated with volumes >6.6 ml.
Similarly, evaluation of ovarian volume on the day of hCG
administration discriminates between women who have mod-
Figure 8.2. Antral follicle count by inversion mode.
possibility of discussing the findings with the patient. To
address this, new software has been developed that can automatically calculate follicle diameter and volume. The
operator simply captures the ovarian volume, and the software
erate versus severe OHSS (271 ± 87 vs. 157.30 ± 54ml) [3].
Evaluating ovarian stroma flow with 3D US
It is possible that poor ovarian vascularization impairs access
of gonadotropin to the ovarian follicles, hampering follicular
68
Chapter 8: 3D Ultrasonography and infertility
Figure 8.3. Ovarian volume calculation through VOCAL software (virtual organ computer-aided analysis) in a patient with low ovarian reserve. Total ovarian volume is 2.5 ml.
growth and d evelopment. Power Doppler US, in combination
with 3D US and VOCAL, is a very good approach for i nvestigating the global ovarian vascular network and its c orrelation with ovarian response in ART. An ovarian vascular
“map” is easily obtained from a sagittal section of the ovary.
It is crucial to avoid patient or US probe movements, as well as
interposition of the bowel, while capturing the volume. Once
captured, vascular flow indexes can be analyzed at a later stage
using software. It should be noted that not all groups report
similar results [2,3,4]. While so me repo rt good c orrelation
between ovarian vascular flow, the number of eggs retrieved,
and better pregnancy rates [5], others have not found such
a correlation. This is most likely due to the very low reduction
in ovarian vascular flow with aging. This decline may not
appear until later, and so may not be useful in early detection
of low responders. Thus, we conclude that investigating
ovarian stroma vascular flow is not an independent tool
for estimating the ovarian response in ART, as it does
not provide additional information to the already known
antral follicle count and ovarian volume evaluation by 2D
US [6,7].
Three-dimensional power Doppler has also been used to
predict oocyte and embryo quality, a key step for successful
ART. The rationale behind this is that adequate follicular vascularization on the day of hCG administration is related to
adequate intrafollicular oxygen concentration, which may facilitate oocyte development and maturation. Low oxygen concentration has been correlated with oocyte cytoplasmic defects and
embryo abnormalities. However, currently there is not enough
evidence to extrapolate data from 3D power Doppler to embryo
development and pregnancy rates.
Evaluating uterine pathology and müllerian anomalies using 3D US
Three-dimensional US has become a key tool for diagnosing
uterine malformations. It has revolutionized this field as it is
noninvasive, reproducible, relatively inexpensive, and well
tolerated compared with techniques such as laparoscopy/hysteroscopy, MRI, or hysterosalpingography (HSG). Threedimensional US is very reliable, since a coronal section can be
obtained, and a septate uterus can now be distinguished from a
69
Section 2: Ultrasonography in infertility
Figure 8.4. SonoAVC software permits both follicular diameter and volume calculation (automated volume calculation). The operator just needs
to capture ovarian volume and the application analyzes and determines diameter as well as volume of the sonolucent areas found.
bicornuate uterus without the need of a laparoscopy. In case of
a septate uterus, 3D US is more accurate than HSG when
estimating the depth of the septum. Multiplanar navigation
allows complete evaluation of the septum and the distance
from the septum to the fundus. If we incorporate 3D power
Doppler, vascularization of the septum can also be determined.
The accuracy of diagnosing septate uteri using 3D US is almost
98% [7].The main sources of error are uterine leiomyomas,
synechiae, or other distorting processes within the cavity.
Diagnosing benign uterine pathologies: endometrial polyps and leiomyomas
Leiomyomas and endometrial polyps are the most frequent
benign uterine pathologies, and both can interfere with the
reproductive process. Three-dimensional US can be used to
precisely establish the size, vascularization and location of myomas and can determine their relation to the endometrial cavity.
At our institution, we recommend removing myomas that distort the endometrial cavity, so 3D US is a valuable tool when
surgery is being discussed. Similarly, 3D US provides a more
reliable postsurgical evaluation of the uterine cavity than 2D US,
avoiding the need for a postsurgery diagnostic hysteroscopy.
The extraordinary capacity of the multiplanar mode to
study the whole endometrium simpli fies identification of polyps, which can hamper embryo implantation if they are larger
than 10mm. The introduction of fluid into the uterine cavity
(for 3D hysterosonography) improves diagnostic accuracy
and is also very useful when evaluating intrauterine synechiae.
The TUI mode provides tomographic sections of the uterus,
permitting global evaluation of the uterus.
Analyzing the endometrium
The human endometrium undergoes intense angiogenesis during the menstrual cycle, and angiogenesis is a key process for
successful embryo implantation and development. Power
Doppler combined with 3D US is a noninvasive way to study
the layers of the whole endometrium using perfusion analysis.
Raine-Fenning et al. [8] investigated changes in endometrial
and subendometrial flow in 27 healthy, fertile volunteers with
regular menstrual periods. They performed 3D power Doppler
on alternate days, starting on cycle D3 until ovulation, and then
every 4 days afterward until initiation of menses. With the use
of VOCAL, the vascular indexes were calculated for each time
point. For the subendometrial vascular index, an arbitrary limit
70
Chapter 8: 3D Ultrasonography and infertility
of 5 mm was established, and the inner third of the endometrium and the area irrigated by radial arteries. They found that
both endometrial and subendometrial vascular flow increased
to a maximum 3 days prior to ovulation, then decreased until
postovulatory D5, and finally began a gradual increase during
the rest of the luteal phase. The proliferative phase increment
was related to estradiol levels and its vasodilating effects, while
the luteal phase increase was related to serum progesterone.
Interestingly, the flow indexes continued to increase during
menstruation regardless of a drastic drop in progesterone levels;
this might be explained by the high endometrial vascular density due to progressive compaction of the spiral arteries. The
reduction in the postovulatory vascular indexes is explained by
vasodilation of the subepithelial capillary plexus, which induces
the required stromal edema to allow embryo implantation.
Jokubkiene et al. [9] condu cted a similar study, finding that
the lowest vascularization index occurred 2 days after ovulatio n
and progressively increased during the luteal phase. Thus, 3D
US is a reliable technique for investigating cyclic, physiological
changes in endometrial vascularization, showing that there are
maximum values 2–3 days prior to ovulation, decreasing to
minimal values 2–5 days postovulation, and increasing thereafter. Vascular flow is delicately orchestrated in order to
provide human embryos a favorable microenvironment for
implantation, although the amount of oxygen the embryo
needs from the endometrium during the implantation process
is still controversial. Some authors believe that a drop in vascularization would induce a relative hypoxia that could facilitate
embryo implantation. However, the increase in vascularization
observed during the days in which implantation takes place
does not support this hypothesis. More studies are needed to
definitively establish the role of endometrial/subendometrial
vascular oscillations in embryo implantation.
The endometrium in infertile women
Evaluation of the endometrium is very important in studying
infertile women. Three-dimensio nal US facilitates noninvasive
evaluation of the human endometrium and identifies some
organic problems that can negatively influence the implantation process [10,11]. Specifically, endometrial volume determination and evaluation of endometrial angiogenesis using
vascularization indexes can easily and accurately be performed
using 3D US.
Endometrial neoangiogenesis may differ in natural cycles
versus stimulated cycles, such as in IVF. The vascularization
indexes are different in fertile women than in patients with
unexplained infertility; the latter show a dramatic decrease in
both endometrial and subendometrial vascularization indexes
that are unrelated to both estradiol or progesterone levels and to
endometrial thickness and volume. This suggests that vascular
dysfunction may compromise embryo implantation [12].
Similarly, vascular changes that take place during natural menstrual cycles have been compared with those that occur in
stimulated cycles. Ng et al. [13] compared vascular changes in
natural and stimulated cycles in the same patient and found a
35% decrease in endometrial and subendometrial vascularization in stimulated cycles.
Endometrial studies in women undergoing ART
Only 30% of embryos transferred into the uterine cavity after
ART successfully implant. In many cases, this may be due to the
embryo, but in other cases, endometrial receptivity may also be
impaired. Prognostic endometrial receptivity markers are still
needed to identify patients with a good, fair, or poor prognosis.
Patients with a good prognosis might benefit from single
embryo transfer, whereas patients with a poor prognosis may
be advised to have the embryo frozen, and transferred at a later
stage in a natural cycle.
Throughout the years, multiple variables relating cycle outcome with endometrial thickness and pattern have been identified based on 2D US assessment of endometrial perfusion at
the uterine, arcuate, radial, and spiral arteries. Endometrial/
subendometrial mapping with color Doppler and power
Doppler has also been used [14,15]. Some have reported a
positive correlation between endometrial thickness, volume
and/or texture and IVF cycle outcome [16,17,18]; others have
not observed this positive correlation [19,20,21]. Two reports
concluded that pregnancy cannot result if the endometrial
volume is less than 1–2ml[16,22].
Initially, pulsed Doppler studies of uterine arteries appeared
extremely promising in terms of determining a cut-off value for
predicting pregnancy, but subsequent studies failed to confirm
this link. This may be due to the lack of correlation between the
uterine artery pulsatility index and endometrial vascularization.
A positive correlation between the subendometrial blood flow
morphology in the spiral arteries and IVF cycle results was also
reported [23], although not all studies supported this conclusion [24].
Three-dimensional US allows prompt, integrated evaluation of all known receptivity markers by measuring endometrial
thickness, texture, pattern, volume, and global perfusion.
Endometrial/subendometrial perfusion provides a more direct
estimate of endometrial receptivity. It has been evaluated in
different phases of the stimulated ART cycle: on the day of hCG
administration [6,22,25,26], the day of egg retrieval [27], and
the day of embryo transfer [16,23]. Some investigators focused
only on endometrial vascularization [6], expecting a close correlation of the implantation process with the tissue in which the
embryo implants. Others also investigated the relationship of
subendometrial vascularization to implantation [7], speculating
that a more favorable environment with better subendometrial
perfusion would positively influence implantation.
There is no generally accepted consensus about the area that
should be studied for adequate assessment of subendometrial
vascularization. While some groups consider 1 mm outside the
endometrium adequate [27], others postulate that a 5 mm [8]or
10 mm margin [26] should be used. The choice of a smaller
margin (i.e., 1 mm) is based on the fact that cyclic changes in
vascularization occur in that region in response to sex steroid
71
Section 2: Ultrasonography in infertility
72
Figure 8.5. Intrauterine vs. cornual pregnancy. On certain occasions, an excessive lateralization of the gestational sac toward the uterine horn may confuse the
operator and prompt a wrong diagnosis of corneal pregnancy. The image in the coronal section (bottom left) enables the visualization of the adequate placement of
the gestational sacs in close contact with the uterine cavity
secretion throughout the cycle. A wider margin may inadvertently include leiomyomas, which could interfere with the accuracy of the indexes. Not unexpectedly, the results of these
studies have been highly variable. Some authors found a direct
relationship between pregnancy rates and subendometrial vascularization (VI, FI, VFI) on the day of hCG administration
[25,28] or on the day of embryo transfer [2], whereas others
found no correlation with the day of hCG [27], or even found
the opposite (a higher pregnancy rate when endometrial/subendometrial flow was absent). Although no differences were
found in patients with a good prognosis, cycle outcome seemed
improved in patients with poor embryo quality but with better
endometrial vascularization (VI, FI, VFI). This was true for invitro fertilization [6,28] as well as for cryopreserved embryo
transfers [29].
Endometrial/subendometrial vascularization may also serve
as a prognostic marker of ongoing pregnancy, as lower perfusion correlates with miscarriages [30]. None of the other study
parameters – endometrial thickness, volume, or texture – had
any predictive value in terms of pregnancy evolution. This
finding may be helpful in order to appropriately counsel
patients with a high chance of miscarriage and also as a guideline for implementing early preventive measures.
In summary, there is currently no reliable ultrasonographic predictor of endometrial receptivity for patients
undergoing ART [31], except for predicting which patients
will have little chance of achieving a pregnancy. Study of the
global endometrial perfusion with 3D power Doppler US
appears very promising . Ho wever, further c omparative studies are needed to establish cut-off values in order for practitioners to counsel patients about their prognosis regarding
endometrial receptivity. Studies performed during the
embryo transfer procedure as well as during the window of
implantation are needed to fully understand the vascular
modifications that take place in the endometrium during
this time. This information might help improve these processes as well as help doctors make informed decisions about
how many embryos to transfer.