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Safety Aspects of Doppler and Color Doppler Sonography
contrast agents during pregnancy, provided they are limited to
the visualization of maternal tissues.
Exposure of Gas-Containing Tissues
Recent studies in various laboratory mammals such as mice,
rabbits, pigs, and monkeys have shown that diagnostic insonation of the lung can induce local extravasation of capillary red
cells if the negative pressure amplitudes is above 1 MPa.
Greater negative pressures are needed to produce this effect in
larger animal species than in small animals. The same effect
has been observed at slightly higher thresholds (ⱕ 2MPa) in
Measures to Limit Risk
Ultrasound field parameters. Users should know the ultra-
sound field parameters in the various modes that are relevant
to clinical safety. International Standard 1157 of the IEC
quires that manufacturers provide users with necessary information on equipment exposure parameters. The German
2
Union of Fund-Affiliated Physicians approves for clinical use
only equipment that conforms to this standard
Some ultrasound equipment displays output indices on the
monitor screen in accordance with the requirements of the
17
.
gas-filled bowel (reviewin reference 20). Apparently this effect
is nonthermal and requires air-filled cavities, and therefore the
fetal lung is not at risk. The underlying mechanism is still unclear,and so far this phenomenon has been seen only in laboratory animals. The capillary bleeding in these cases was so slight
that it would not be detectable by clinical examination in
humans. It is not known whether the human lung, with its
greater alveolar size, is at risk. Evidence acquired to date does
not support the need to revise the indication for diagnostic ultrasound. Nevertheless, it is a good precaution to avoid unnecessary ultrasound exposure to gas-containing organs like the
lung and bowel. Ultrasound should not pose a danger to the
nonaerated fetal lung.
Output Display Standard (ODS)
16
re-
given appropriate information in advance in order to interpret
the indices that are displayed (thermal index TI and mechanical index MI)
Training. A final essential aspect of risk abatement is the qualified training of examiners. This applies both to the risk-free
use of diagnostic ultrasound equipment and to the avoidance
of diagnostic errors.
9
.
2
. However, the user must be
32
Recommendations
Various national and international institutions have published
recommendations on the prevention of health risks from diagnostic ultrasound
assumed that the ultrasound energy transmitted into the body
should be kept low as a precautionary measure, even if bioeffects are not expected to occur. The recommendations are
summarized below.
General Recommendations
1. The power output of ultrasound equipment should be as
low as possible, and the gain should be set as high as
possible.
2. The operator should know whether the equipment continues to emit ultrasound in the freeze-frame mode and, if
necessary, should break transducer–skin contact.
3. Ultrasound examinations should be medically indicated.
There are no safety objections to the routine B-mode ultra-
sound screening of all pregnancies.
4. Air-containing organs such as the lung, stomach, and bowel
should not be exposed unnecessarily to ultrasound.
5. The use of ultrasoundcontrast agents requires a definite in-
dication. Their use should be preceded by an individual
risk–benefit analysis for the patient.
1,22, 24, 25
. In all of these recommendations, it is
Pulsed Doppler
6. Pulsed Doppler for flowmetry should be activated only
after the vessel of interest has been identified with color
Doppler and the sample volume (range gate) has been defined. The sample volume should be kept small, because
some instruments compensate for attenuation with time
gain compensation (TGC) even in the pulsed Doppler
mode.
7. In fetal and neonatal examinations, exposure of bone
below the region of interest should be minimized or
avoided.
8. The Doppler scan time should be kept short to avoid
possible excessive heating and should not exceed 30 seconds if possible. Repeat sampling, if necessary, should be
done after a delay of 60 seconds.
9. Fever potentiates the thermal risk, and therefore a shorter
scan time should be used in febrile patients.
10. Routine screening of the fetal and placental circulation
with Doppler ultrasound cannot be recommended for
every pregnancy owing to continued uncertainties about
risks.
Appendix: Statements on the Biological Safety of Diagnostic Ultrasound Fields
Appendix: Statements on the Biological Safety of Diagnostic Ultrasound Fields
Ultrasound exposure during pregnancy. The embryonic period
EFSUMB Statement on the Clinical Safety of Diagnostic Ultrasound
Diagnostic ultrasound has been widely used in clinical medicine for many years with no proven deleterious effects.
However, as the use of ultrasound increases, with the introduction of new techniques, with a broadening of the medical indications for ultrasound examinations, and with increased exposure, continuous vigilance is essential to ensure its continued safe use.
A broad range of ultrasound exposure is used in the different diagnostic modalities currently available. Doppler imaging
and measurement techniques may use higher exposures than
those used in B- and M-modes, with pulsed Doppler techniques having the potential for the highest levels.
The recommendations contained in this statement assume
that commercial ultrasound equipment conforming to international safety standards is being used, and that it is used prudently, by competent personnel who are trained in safety matters.
B- and M-modes. Based on scientific evidence of ultrasoundinduced biological effects to date, there is no reason to
withhold B- or M-mode scanning for any clinical application,
including the routine clinical scanning of every woman during
pregnancy. Some techniques, such as tissue harmonic imaging
and coded excitation, may use higher exposures than conventional imaging. The user is advised to monitor the TI and MI
values on the screen and to avoid unnecessarily high values
and prolonged exposure times. Scanning for 3 D imaging does
not introduce any additional safety considerations.
Doppler modes (color flow, power Doppler imaging and spec-
tral pulsed Doppler). Exposures used in these Doppler modes
are commonly higher than for B- and M-modes. The highest
powers, and therefore the greatest potential for thermal effects, occur in spectral pulsed Doppler mode at high settings of
the output power and scale controls and in Doppler imaging
modes when using narrow or deep color boxes.
The informed use of Doppler ultrasound is not contraindicated. However, at maximum machine output settings, significant thermal effects at bone surfaces cannot be excluded. The
user is advised to monitor the TI and MI (mechanical index)
values on the screen, and to act prudently to limit these, and
exposure times, when scanning sensitive structures and regions of bone and gas.
10
is known to be particularly sensitive to any external influences.
Until further scientific information is available, investigations
should be carried out with careful control of output levels and
exposure times.
With increasing mineralization of the fetal bone as the fetus
develops, the possibility of heating fetal bone increases. The
user should prudently limit exposureof critical structures such
as the fetal skull or spine, particularly during Doppler studies.
Safety considerations for other organs. Particular care should
be taken to reduce the risk of heating during investigations of
the eye. Extra care is also appropriate when carrying out
neonatal cardiac and cranial investigations.
(1994, revised 1998, 2002, and 2003)
WFUMB Statement on Thermal Effects in Clinical Applications
B-mode imaging. Known diagnostic ultrasound equipment, as
used today for simple B-mode imaging, operates at acoustic
outputs that are not capable of producing harmful temperature
rises. Its use in medicine is, therefore, not contraindicated on
thermal grounds. This includes endoscopic, transvaginal and
transcutaneous applications.
Doppler. It has been demonstrated in experiments with unperfused tissue that some Doppler diagnostic equipment has the
potential to produce biologically significant temperature rises,
specifically at bone–soft tissue interfaces. The effects of ele-
vated temperatures may be minimized by keeping the time for
which the beam passes through any one point in tissue as short
as possible. Where output power can be controlled, the lowest
available power level consistent with obtaining the desired diagnostic information should be used. Although the data on
humans are sparse, it is clear from animal studies that exposures resulting in temperatures less than 38.5⬚C can be used
without reservation on thermal grounds. This includes obstetric applications.
Transducer heating. Asubstantial source of heating may be the
transducer itself. Tissue heating from this source is localized to
the volume in contact with the transducer.
(1991, revised 1996)
25
References
Physical and Technical Principles
Doppler for fetal heart monitoring (CTG). The power levels
used for fetal heart monitoring (CTG) are sufficiently low that
the use of this modality is not contraindicated on safety
grounds, even when it is to be used for extended periods.
Gas-filled contrast agents. Particular safety considerations are
associated with the use of gas-filled contrast agents. High
values of mechanical index should be used only when required
for a particular clinical study.
1 American Institute of Ultrasound in Medicine (AIUM): Bioeffects Con-
siderations for the Safety of Diagnostic Ultrasound. AIUM, Bethesda
Md. 1988
2 American Institute of Ultrasound in Medicine and National Electrical
Manufacturers Association (AIUM/NEMA): Standard for Real Time
Display of Thermal and Mechanical Acoustic Output Indices on Diagnostic Ultrasound Equipment. AIUM, Rockville Md. 1992
3 Barnett SB, Rott H-D, Ter Haar G, Ziskin MC, Maeda K, Nyborg W: The
sensitivity of biological tissue to ultrasound. Ultrasound Med. Biol. 23
(1997) 805–812
33
Safety Aspects of Doppler and Color Doppler Sonography
4 Bosward KL, Barnett SB, Wood AKW, EdwardsMJ, Kossoff G: Heating of
guinea–pig fetal brain during exposure to pulsed ultrasound. Ultrasound Med. Biol. 19 (1993) 415–424
5 Carstensen EL, Child SZ, Norton S, Nyborg WL: Ultrasonic heating of
the skull. J. Acoust. Soc. Am. 87 (1990) 1310–1317
6 Duck FA, Martin K: Trends in diagnostic ultrasound exposure. Phys.
Med. Biol. 36 (1991) 1423–1432
7 European Committee for Ultrasound Radiation Safety—The Watch-
dogs: Tutorial Paper: Transvaginal ultrasonography—Safety aspects.
Eur. J. Ultrasound 1 (1994) 355–357
8 European Federation of Societies for Ultrasound in Medicine and Biol-
ogy (EFSUMB): Guidelines for the safe use of Doppler ultrasound for
clinical applications. Eur. J. Ultrasound 2 (1995) 167–168
9 European Federation of Societies for Ultrasound in Medicine and Biol-
ogy (EFSUMB): Tutorial Article: Thermal and mechanical Indices. Eur.
J. Ultrasound 4 (1996) 145–150
10 European Federation of Societies for Ultrasound in Medicine and Biol-
ogy (EFSUMB): Clinical Safety Statement for Diagnostic Ultrasound
2003. EFSUMB Newsletter 17(1) (2003) 15
11 European Federation of Societies for Ultrasound in Medicine and Biol-
ogy (EFSUMB): Tutorial: Thermal teratology. Eur. J. Ultrasound 9
(1999) 281–283
12 European Federation of Societies for Ultrasound in Medicine and Biol-
ogy (EFSUMB): Tutorial: Acoustic cavitation and lung haemorrhage.
Eur. J. Ultrasound 9 (1999) 277–280
13 European Federation of Societies for Ultrasound in Medicine and Biol-
2
ogy (EFSUMB): Tutorial: Safety of ultrasonic contrast agents. Eur. J. Ultrasound 9 (1999) 195–197
14 Henderson J, Willson K, Jago JR, Whittigham TA: A survey of the acous-
tic outputs of diagnostic ultrasound equipment in current clinical use.
Ultrasound Med. Biol. 21 (1995) 699–705
15 Heusinger H: Comparison of the reactions induced by ultrasound and
gamma rays in aqueous lactose solutions. Ultrasonics 28 (1990) 30–36
16 International Electrotechnical Commission (IEC): International Stan-
dard 1157: Requirements for the Declaration of the Acoustic Output of
Medical Diagnostic Ultrasonic Equipment. Genf 1992
17 Kassenärztliche Bundesvereinbarung (KBV): Qualitätsvoraussetzun-
gen gemäß § 135 Abs. 2 SGB V zur Durchführung von Untersuchungen in der Ultraschalldiagnostik (Ultraschallvereinbarung) vom
10.02.1993. Dtsch. Arztebl. 90 (1993) B390–403
18 Nanda NC: Echocontrast enhancers – how safe are they? Advances in
Echo Contrast 2 (1993) 97–110
19 National Council on Radiation Protection and Measurements (NCRP):
Exposure Criteria for Me dical Diagnostic Ultrasound: I. Criteria based
on Thermal Mechanisms. NCRP Report No 113, Bethesda Md. 1992
20 Rott H-D: Capillary lung bleeding from exposure to diagnostic ultra-
sound – A literature review. BMUS Bullentin 5 (1997) 20–21
21 Rott H-D: Ultraschalldiagnostik: Neuere Bewertung der biologischen
Sicherheit. Dtsch. Arztebl. 93 (1996) A1533–1537
22 Strahlenschutzkommission (SSK) des Bundesministeriums für Um-
welt, Naturschutz und Reaktorsicherheit: Empfehlungen zur
Patientensicherheit bei Anwendungen der Ultraschalldiagnostik in
der Medizin. Empfehlungen der Strahlenschutzkommission (Heft 14).
Empfehlungen und Dokumentationsteil. Fischer, Stuttgart 1998
23 Ter Haar GR, Duck FA, Starritt HC, Daniels S: Biophysical characterisa-
tion of diagnostic ultrasound equipment – preliminary results. Phys.
Med. Biol. 34 (1989) 1533–1542
24 World Federation for Ultrasound in Medicine and Biology (WFUMB):
Symposium on Safety and Standardisation in Medical Ultrasound: Issues and Recommendations Regarding Thermal Mechanisms for Biological Effects of Ultrasound. Barnett SB, Kossoff G (eds.): Ultrasound
Med. Biol. 18/9 (Special Issue) 1992
25 Barnett SB, Ter Haar GR, Ziskin MC, Rott HD, Duck FA, Maeda K: Inter-
national recommendations and guidelines for the safe use of diagnostic ultrasound in medicine. Ultrasound Med. Biol. 26 (2000) 355–66
34
Infertility Evaluation and
Assisted Reproduction
3 Uterine Blood Flow in Fertile and Infertile Women
S. Kupesic and A. Kurjak
Uterine Blood Supply
Anatomy. The uterus derives most of its blood supply from the
uterine arteries, with a small amount supplied by the ovarian
arteries. The uterine arteries branch into the arcuate arteries
(Fig. 3.
1), which project circumferentially into the outer third
of the myometrium. The arcuate arteries divide further into the
radial arteries, which then branch into the basal arteries and
spiral arteries after crossing the myometrial–endometrial
boundary. The relatively short basal arteries terminate in a
capillary bed that supplies the stratum basale of the endometrium. The spiral arteries project farther into the en-
3
dometrium and open into a broad capillary bed that supplies
the stratum functionale of the endometrium.
Menstrual cycle. Interestingly, only the spiral arteries show demonstrable anatomical changes during the menstrual cycle
These arteries contract when menstruation occurs, possibly as
a result of falling estrogen and progesterone levels. This vasoconstriction induces local hypoxia, ischemia, and cell death in
the stratum functionale. The distal portion of the arteriolar
vascular bed and the capillary bed are then sloughed along
with the stratum functionale. The basal arteries do not react to
falling estrogen and progesterone levels and thus serve to
maintain the integrity of the stratum basale during the menstrual cycle
ness occurs during the next menstrual cycle. To ensure this, a
completely new capillary bed arises from the rapidly growing
proximal portions of the spiral arteries. The process begins
with the growth of new capillaries from the stratum basale
new intima and muscular coat develops in the capillary walls
Implantation. The angiogenesis that occurs during the proliferative and secretory phases of the menstrual cycle serves to
12
. A 3-fold to 5-fold increase in endometrial thick-
24
.
Fig. 3.1 Transvaginal image of an arcuate arterial network.
prepare the endometrium for the implantation of a fertilized
13
ovum
with the attachment of the blastocyst to the endometrial surface. As the trophoblastic cells invade the endometrium, maternal capillaries are breached, causing profound physiological
and structural changes to occur in the uterine vascular bed
One of the first changes is increased vascular permeability at
12
.A
20
the implantation site
tion of the endometrium in preparation for angiogenesis
sequent placentation is facilitated by the changes in the mater-
.
nal vascular bed. Further details on this process can be found in
the section on the Doppler examination of early placentation
and embryonic blood flow (p. 103).
. After fertilization has occurred, implantation begins
Changes in Uterine Blood Flow during the Menstrual Cycle
3
. This is followed by a metabolic activa-
3
. Sub-
21
.
36
More than any other available examination technique, transvaginal color Doppler sonography requires an accurate knowledge of the location of the uterus, myometrium, endometrium,
and the vessels that supply them
It is known that uterine perfusion depends largely: on the
age of the patient, the phase of the menstrual cycle, and other
special factors such as pregnancy or neoplasia
will be analyzed below in detail.
5, 11, 17, 18
.
19
. These factors
Blood Flow Parameters in the Uterine Arteries
Complex relationships exist between ovarian hormone levels
in the peripheral venous blood and the blood flow parameters
in the uterine arteries
small amount of end-diastolic blood flow can be detected in
the uterine arteries in the majority of women (Fig.3.
sistance index (RI) until day 13 of a 28-day cycle is in the range
0.88 ⫾ 0.04. Steer et al.
2, 8, 9, 23
. During the proliferative phase, a
2). The re-
23
reported that diastolic flow was no
Changes in Uterine Blood Flow during the Menstrual Cycle
Fig. 3.2 The uterine artery appears to the left of the cervix at the
junction of the cervix and uterine corpus. The blood flow velocity in
the uterine artery during the proliferative phase is characterized by
low end-diastolic blood flow and a high vascular resistance (RI = 0.87).
longer detectable in the uterine arteries on the day of ovulation. Goswamy and Steptoe
8
found an increasing resistance
index and systole/diastole ratio during the postovulatory fall in
serum estradiol levels. Increased resistance in the uterine arteries was measured three days after the surge in luteinizing
hormone (LH), and Scholtes et al.
22
found that the pulsatility
index (PI) in the uterine arteries was highest on day 16 of the
menstrual cycle.
These results could be due to increased uterine contractil-
10
ity
and increased compression of the vessels traversing the
uterine wall, thus reducing the vessel diameters and causing
greater flow resistance. During the normal menstrual cycle, a
sharp rise of end-diastolic blood flow velocities can be demonstrated between the proliferative and secretory phases
18
.Itis
particularly noteworthy that the lowest vascular resistance
coincides with the period of maximal corpus luteum function
(RI = 0.84 ⫾ 0.04), when implantation most commonly occurs
(Fig. 3.
3). It seems logical that the blood flow to the uterus is
highest in the luteal phase, and this increase has been reported
by Kurjak et al.
1
et al.
. The persistence of a low RI in the luteal phase suggests
18
, Goswamy et al.
8, 9
, Steer et al.23, and Bataglia
that the relaxation effect on the uterine arteries continues
until the start of menstruation. Zaidi et al.
27
described a circadian rhythm in uterine artery blood flow, independent of
fluctuating hormone levels.
Fig. 3.3 The blood flow velocity in the uterine artery during the
secretory phase is characterized by a higher velocity and lower resistance index (RI = 0.81).
Infertility Evaluation and Assisted Reproduction
Fig. 3.4 Doppler trace of the right radialarteries. Note the position of
the cursor in the left half (in the myometrium) for sampling the Doppler spectrum. Lower velocities and a lower resistance (RI = 0.69) are
measured in the examined vessels.
Blood Flow Parameters in the Radial and Spiral
Arteries
Blood flow fluctuations similar to those in the main trunk of
the uterine artery were observed in the radial and spiral arteries following the introduction of transvaginal color Doppler
and pulsed Doppler sonography
that the postovulatory fall of serum estradiol levels coincides
with a postovulatory rise of the RI in the myometrial vessels
(Fig. 3.
5).
14
(Fig. 3. 4). Our results show
Fig. 3.5 Blood flow velocities in the radial arteries during the periovulatory period. The suspension of end-diastolic blood flow (right) is a
transient effect based on myometrial contractions.
37
Uterine Blood Flow in Fertile and Infertile Women
Fig. 3.6 Color signals from the spiral arteries in the periphery of the
three-line endometrium.
It has been shown that increased uterine contractility is as-
sociated with a decrease in endometrial blood flow
10
.Itiswell
known that the endometrium undergoes marked structural
and functional changes during the menstrual cycle. The histo-
3
logical changes include a remarkable degree of new blood vessel formation (Fig.3.
6). The spiral arteries show increased
development during the menstrual cycle. The increase in endometrial blood flow depends strongly on the blood flow in the
uterine artery, arcuate arteries, and radial arteries. When the
Uterine Blood Flow in Infertile Women
As more experience is gained with transvaginal color and
pulsed Doppler ultrasound, this examination has assumed an
important role in the management of infertile women. A
steadily increasing RI has been measured in the uterine arteries during anovulatory cycles (Fig. 3.
8). Moreover, end-dias-
Fig. 3.7 Blood flow velocities in the spiral arteries during the periovulatory period. A scan on the day of ovulation shows a decreased resistance index (RI = 0.50) and increased blood flow velocity.
spiral arteries in a normal cycle are compared with the uterine
arteries, which have larger diameters, the spiral arteries are
found to exhibit lower blood flow velocities (p ⬍ 0.05) and a
lower vascular resistance (p ⬍ 0.05) (Fig. 3.
7). It appears that
the data obtained by analyzing endometrial blood flow permit a more accurate assessment of the success rate of implantation and of unexplained fertility problems than the
evaluation of uterine artery blood flow alone.
tolic blood flow cannot be detected in some infertile women
(Fig. 3.9). The data are still insufficient, however, to establish
whether absent end-diastolic blood flow is associated with infertility and low pregnancy rates.
9
38
1.00
RI
0.98
0.96
0.94
0.92
0.90
0.88
0.86
0.84
0.82
0.80
5
Fig. 3.8 Uterine artery blood flow changes in fertile and infertile
women during the menstrual cycle.
Infertile women with anovulatory cycles, n=28
Fertile women
****
7 9 11 13 15 17 19 21 23 25 27
*p<0.05
Day of menstrual cycle
Fig. 3.9 Absence of end-diastolic blood flow in both uterine arteries
in a patient with primary infertility.
Uterine Blood Flow in the Normal Cycle and during Ovarian Stimulation with Confirmed Ovulation
Uterine Blood Flow and Fertilization Rate
The assessment of uterine artery blood flow could be used as a
means of detecting unfavorable uterine blood flow before a
planned embryo transfer.
Steer et al.23calculated the likelihood of pregnancy on the day of
embryo transfer based on pulsatility values in the uterine arteries.
According to their findings, the likelihood of pregnancy was
greatest when medium PI values were measured in the uterine
artery. In 35% of cases, pregnancy did not occur when the mean PI
value before the embryo transfer was greater than 3.0.
Tsai et al.
sion on the day of human chorionic gonadotropin (hCG) adminis-
tration in patients who were undergoing intrauterine insemination.
They calculated the PI of the ascending branch of the uterine artery
on the day of hCG administration and compared the vascular resistance in the uterine artery with the outcome of intrauterine insemination. No pregnancy occurred when the PI was greater than
3. The fertilization rate was 18% when the PI was less than 2 and
19.8% when the PI was between 2 and 3. These data indicate that
the measurement of uterine perfusion on the day of hCG adminis-
tration may be of value in predicting the success of intrauterine insemination.
Zaidi et al.
artery blood flow by transvaginal color Dopplerscanning on the day
of hCG administration in patients undergoing in-vitro fertilization
(IVF) could predict pregnancy and implantation rates. One hundred
thirty-five patients undergoing 139 IVF cycles were analyzed. The
results of the study suggest that the measurement of the uterine
artery PI on the day of hCGadministration can predict the likelihood
of successful implantation, since the highest pregnancy rate
(34.7%) was associated with a uterine artery PI between 2 and 3. If
possible, hCG should be administered when the uterine artery PI is
less than 3 in order to achieve a high implantation rate.
Further studies are needed, however, to investigate the precise
relationship between uterine artery blood flow and the likelihood of pregnancy. In embryo-transfer patients who are found
to have unfavorable uterine blood flow indices, it might be prudent to freeze the embryos and reschedule the transfer for a
later date. It may b e possible to improve uterine blood flow by
administering estradiol
25
investigated the prognostic value of uterine perfu-
28
investigated whether the assessment of uterine
6
or progesterone4.
Endometrial Imaging
One of the greatest problems in the current practice of in vitro
fertilization is the transfer of multiple embryos in an effort to
increase the pregnancy rate. This leads to an increased number
of multiple pregnancies, which are associated with poorer perinatal outcomes and higher obstetric risks than singleton pregnancies. It is known that the likelihood of pregnancy depends
strongly on the embryo itself and on favorable uterine blood
flow. Instead of performing an endometrial biopsy, which can
lead to injury and bleeding at the implantation site, color
Doppler sonography can be used as a means of detecting
favorable uterine blood flow
Zaidi et al.26examined 96 patients undergoing IVF treatment on
the day of hCG administration by transvaginalcolor Doppler sonography. They assessed endometrial thickness, endometrial morphology, the presence or absence of subendometrial or intraendometrial blood flow, and intraendometrial vascular penetration on
the day of hCG administration and related the results to pregnancy
rates. The overall pregnancy rate was 32.3%. There were no significant differences between the pregnant and nonpregnant groups
with regard to endometrial thickness, subendometrial peak systolic
blood flow velocity, or subendometrial pulsatility index. However,
the absence of subendometrial blood flow was always associated
with a failure of implantation.
16
.
Conclusions
Transvaginal color and pulsed Doppler sonography is a highly
reproducible study that is fast and easy to perform. It may predict the likelihood of successful implantation, thereby reducing the incidence of multiple gestation. The measurement of
uterine blood flow could provide a noninvasive tool for investigating the uterine milieu and could help us to learn more about
the pathophysiology of infertility, especially in cases with an
undetermined cause.
Infertility Evaluation and Assisted Reproduction
Uterine Blood Flow in the Normal Cycle and during Ovarian Stimulation with Confirmed
Ovulation
Kupesic and Kurjak27measured blood flow velocities in the uterine,
radial, and spiral arteries during the periovulatory period of normal
cycles and in stimulated cycles with confirmed ovulation. Seventyeight patients with a male infertility factor were examined daily in
an IVF clinic. In normal cycles, the uterine artery PI was 3.16 two
days before ovulation and decreased to 2.22 on the day before ovulation. This difference was not observed in stimulated cycles. The
mean PI was 3.06 and remained unchanged during the periovula-
tory period. Distinct waveforms could be recorded from the endometrium and myometrium during this period. The PI in the radial
and spiral arteries showed higher values in stimulated cycles than in
normal cycles.
Clomiphene citrate. It is known that clomiphene citrate occupies
the estrogen receptors in estrogen-sensitive tissues and in this way
influences the growth of the endometrium
was found between endometrial thickness and blood flow veloci-
ties. This did not apply to the patient group that had received
clomiphene citrate/human menopausal gonadotropin (hMG)
stimulation and exhibited normal endometrial development. The
authors found absent end-diastolic blood flow in the spiral arteries
in 55.6 % of these cases (Fig. 3.10). No differences in endometrial
thickness or perfusion were seen between the hMG-stimulated
patients and the nonstimulated patients with normal cycles.
7
. A strong correlation
39
Uterine Blood Flow in Fertile and Infertile Women
Fig. 3.10 Blood flow velocities in the spiral arteries of a triple-line en-
dometrium (left). The absence of end-diastolic blood flow is a sign of
poor endometrial perfusion and correlates with poor endometrial re-
ceptivity.
Conclusion. Blood flow changes in the spiral arteries can be
considered an accurate predictor of implantation success rates
in patients undergoing IVF and embryo transfer. In patients
3
who are found to have unfavorable uterine blood flow in the
current treated menstrual cycle, the embryos should be frozen
and the transfer postponed for a normal cycle or a cycle with
favorable endometrial blood flow in response to therapy.
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11 Jurkovic D, Jauniaux E, Kurjak A, Cambell S: Transvaginal color Doppler
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Gynaecol. 93 (1986) 1049–1059
14 Kupesic S, Kurjak A: Uterine and ovarian perfusion during the peri-
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23 Steer CV, Mills CV, Campbell S: Vaginal color Doppler assessment on
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24 Torry RJ, Rongish BJ: Angiogenesis in the uterus: potential regulation
and relation to tumor angiogenesis. Am. J. Reprod. Immunol. 27 (1992)
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381
40
4 Uterine Causes of Infertility
S. Kupesic and A. Kurjak
For fertilization to occur, the uterine cavity must create an optimum environment for the successful transport of spermatozoa from the cervix tothe fallopian tubes. A normal structure of
the uterine mucosa, with normal glandular secretions and
blood flow, is also essential for implantation and placentation.
Uterine abnormalities such as polyps, leiomyomas, malignant
tumors, infections, and intrauterine adhesions and synechiae
Ultrasound Detection of Uterine Abnormalities
Congenital Anomalies
Congenital anomalies of the uterus are diagnosed in 38–55 % of
women with habitual abortion
Examination during the secretory phase. The ultrasound diagnosis of uterine anomalies such as a septate uterus, bicornuate
uterus, or uterus didelphys is most sensitive and specific
during the secretory phase of the menstrual cycle. The accuracy of the ultrasound diagnosis depends on the severity of
the anomaly
during the secretory phase, when separate echogenic lines demarcate the endometrium from the surrounding hypoechoic
myometrium, making it easier to detect contour abnormalities
(Fig. 4.
1). Accordingly, a careful transvaginalultrasound exami-
nation in a patient with a unicornuate uterus can demonstrate
a single uterine cornu with an atypical endometrial echo
23
. The endometrium is most clearly defined
33, 47
.
24
.
can contribute to fertility problems. Accordingly, numerous
studies have been done to look for a correlation between sono-
graphic parameters (endometrial thickness and echogenicity)
and uterine receptivity to conception. This chapter explores
the role of transvaginal and color Doppler sonography in evaluating endometrial changes during the menstrual cycle and in
the detection of uterine abnormalities.
Large intracavitary fluid collections should raise suspicion of
hymenal or even vaginal atresia.
Sonohysterography. Sonohysterography refers to the continuous sonographic visualization of the uterine cavity during and
after the instillation of contrast medium into the uterus
method can accurately demonstrate uterine septa, for example, and can define their extent. In a study by Randolph et
41
al.
, the results of sonohysterography agreed with hysteroscopic findings in 53 of 54 patients, corresponding to a sensitivity of 98 % and a specificity of 100%.
The interested reader can find more information on the ultrasound and color Doppler evaluation of uterine anomalies in
Chapter 26 (p. 259 –265).
11
. This
Endometrial Polyps
Endometrial polyps are known to have causal significance in
habitual abortion and infertility. The polyps appear sono-
graphically as diffuse or focal sites of endometrial thickening.
On sonohysterography, an intracavitary polyp appears surrounded by echo-free fluid, and its site of attachment can generally be identified
in the follicular phase of the cycle, it is unnecessary to instill
fluid in order to detect increased endometrial thickness
(Fig. 4.
3). Generally, however, polyps can be detected more
11
(Fig. 4.2). If the examination is performed
Infertility Evaluation and Assisted Reproduction
Fig. 4.1 Uterine duplication anomaly demonstrated by transvaginal
color Doppler sonography. Two separate endometrial images can be
seen during the secretory phase of the menstrual cycle.
fluid instillation.
The use of transvaginal color Doppler sonography makes it
possible to identify small arteries that supply the endometrial
polyps (Fig. 4.
curate examination of the uterine cavity in which the polyps
can be clearly visualized and delineated from the uterine wall
(Fig. 4.
5).
4). Three-dimensional ultrasound permits an ac-
41