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112
Color Doppler Sonography in Ectopic Pregnancy
Transvaginal Color Doppler Sonography
Typical Findings in Normal and Ectopic
Pregnancy
Typical Doppler features of the peritrophoblastic region. With
the increasing clinical use of transvaginal color Doppler sonography, studies began to be published in the early 1990 s dealing
with the circulatory patterns that are typically found in association with early placentation
peritrophoblastic region displayed typical Doppler features
characterized by a high systolic flow velocity, low impedance,
and a high diastolic flow velocity. This suggested the presence
of a high pressure gradient between a maternal artery and a
perfused area under low pressure, the intervillous space. The
normal histomorphological correlate is found in the maternal
vessels at the site of placentation. With an ectopic implantation, corresponding signs of early placentation are found until
the limitations of the abnormal implantation site put an end to
the process and (barring onset of an acute disease process) regressive changes become predominant.
12
Decreased pulsatile flow in the fallopian tube. When the blastocyst implants into the tubal mucosa, the trophoblast infiltrates the lamina propria of the mucosa and the muscular layer
and grows chiefly between the tubal lumen and the serosa, enlarging in the circumferential and longitudinal directions. The
vasotropic growth and the invasion of the surrounding vessels,
the branches of the uterine and ovarian arteries, leads to
greatly increased blood flow and/or intratubal and extratubal
hemorrhage. As a result of this, the ectopic pregnancy reduces
the normally pulsatile blood flow with a high perfusion resistance in the fallopian tube. These hemodynamic changes
can be demonstrated by selective color Doppler imaging of the
tube. Of course, these resistance changes can also be detected
by pulsed Doppler sonography alone, but without direct vascular imaging the Doppler velocimetry scan is time-consuming,
fraught with uncertainties, and therefore impractical in urgent
cases. Color Doppler can provide a rapid and precise “probe.” If
a suspicious anatomical structure has been detected in the
lower pelvis with transvaginal ultrasound, the color-flow
image will yield further information on the hemodynamics at
the site and permit the targeted sampling of flow-velocity
waveforms and their analysis using Doppler indices.
Diagnostic Efficiency
An analysis of the diagnostic efficiency of current methods for
detecting ectopic pregnancy has shown that the added use of
color Doppler improves the diagnostic efficiency of transvaginal ultrasound from 84–95%
pears small, and a comparison of the study conditions used by
different authors makes it difficult to draw a clear positive conclusion.
True-positive and false-positive diagnoses. An important clinical issue is the confidence with which a suspected ectopic
5
. Taylor et al.12found that the
4, 11
to 87–96 %
3, 13
. The gain ap-
pregnancy can provide a primary indication for laparoscopy.
The accuracy of the preoperative presumptive diagnoses compared with the actual findings is expressed by the rate of truepositive and false-positive cases. True validation is not possible
with this type of analysis, because true-negative cases do not
lead to laparoscopy, while false-negative cases take time to
produce overt clinical signs, providing at best a secondary indication for intervention. These include the rather frequent
cases in which curettage is done for a presumed nonviable
early pregnancy (incomplete abortion or blighted ovum) and a
trophoblast is not found in the curettage material. They also include cases of early pregnancy loss, ectopic pregnancies that
are not initially recognized, and the occasional cases with a
poorly vascularized, involuting ectopic pregnancy
1
. Meyers et
al. studied the degree of vascularity as a function of trophoblastic activity as measured by the serum hCG level. They
found a statistical association b etween avascularity and hCG
levels that were low or fell below 1000 IU/l
6
. This observation
should prompt further prospective comparative studies.
Highly acute disease states that warrant immediate action
without comprehensive prior tests are also inaccessible to
validation.
Author’s Studies
In a kind of historical comparison, wereviewed the quality of indica-
tions for laparoscopy in patients with ectopic pregnancy. Our retrospective analysis covered 263 patients who underwent laparoscopy
during a four-year period before the advent of color Doppler-assisted vaginal sonography. These cases were compared with 60 laparoscopies for ectopic pregnancy during a one-year period in
which the primary workup included color Doppler sonography. The
results of the comparison are shown in Fig. 12.1 and Table 12.1.An
improvement in positive predictive value from 91.6% to 95 % indicates a slight increase in the confidence level for laparoscopy referral. The rate of false-positive diagnoses fell from 8.4 % to 5 %, representing only a slight improvement.
The corpus luteum as a major source of error. Critical analysis
reveals that the causes of misdiagnoses have remained the
same. The ultrasound visualization and interpretation of the
corpus luteum led to errors in both the old and new study
populations. Profuse luteal hemorrhage, torsion, ruptures with
intraperitoneal blood collections, and painful sonopalpation of
the adnexal mass and blood-filled cul-de-sac are findings that
strongly bias the clinical decision-making process toward
operative intervention.
Kurjak and his group
patients with intrauterine and ectopic pregnancies and in nonpregnant subjects during the second phase of the menstrual
cycle. They could detect no qualitative difference in perfusion.
In 86.4 % of the patients with ectopic pregnancy, they found
that the corpus luteum and pregnancy were on the same side
of the adnexa. While this observation can be helpful in locating
the ectopic pregnancy, it should also serve as a warning against
false security because of the potential for internal and external
migration of the blastocyst.
10
investigated luteal blood flow in
Transvaginal Color Doppler Sonography
EP laparoscopies after
vaginal sonographic
diagnosis without
color Doppler (n=263)
22 False-positives
= 8.4%
241 True-positives
= 91 .6 %
EP laparoscopies after
vaginal sonographic
diagnosis with
color Doppler (n=60)
3 False-positives
= 5.0%
57 True-positives
= 95.0 %
Fig. 12.1 Diagnostic quality of transvaginal sonographic examina-
tions without color Doppler and with color Doppler in cases of sus-
pected ectopic pregnancy (EP).
Table 12.1 Diagnostic quality of transvaginal sonographic examinations without color Doppler and with color Doppler
Vaginal ultrasound without
color Doppler
Vaginal ultrasound with
color Doppler
3
PI
2
1
0
Uterine artery
(contralateral)
Uterine artery
(EP)
Median
10–90%
Min./Max.
Peritrophoblastic
vessels
Fig. 12.2 Perfusion resistance of uterine and peritrophoblastic tubal
vessels in ectopic pregnancy.
Obstetric Ultrasound
True positive, 241 cases 91.6% True positive, 57 cases 95%
False-positive, 22 cases 8.4 % False-positive, 3 cases 5 %
Partial/complete torsion
with large corpus
luteum of pregnancy
Large hemorrhagic
corpus luteum
Early pregnancy loss,
corpus luteum
Early pregnancy, not
4 Early pregnancy loss,
hemorrhagic corpus
luteum
7 Early pregnancy loss,
corpus luteum
7 Early pregnancy, not
diagnosed
4
1
1
1
diagnosed
Positive predictive value 91.6% Positive predictive
95%
value
It is important to note that the suspicious adnexal structure
must be extraovarian in its location for the acquisition of useful
color flow signals. The very rare cases of ovarian implantation
(⬍1%) should also be considered in this regard.
Pulsatility index. We also determined perfusion resistance based
on the pulsatility index (PI) of the uterine arteries and, where
possible, color-flow signals recorded from the suspicious adnexal
structure. Our goal was to assess and compare the flow impedance
of the uterine artery on the side of the ectopic pregnancy and on
the opposite side and also in the peritrophoblastic vessels. The re-
sults are shown in Fig. 12.2. We found no significant difference be-
tween the resistance indices of the uterine arteries. The mean PI
values, at 1.8 and 1.9, were not significantly different. The median
PI value in the peritrophoblastic tubal tissue was 0.38 and thus significantly lower than in the uterine arteries (p ⬍ 0.01). The indices
for the uterine arcade and spiral arteries in intact intrauterine pregnancies are in the same range, signifying comparable perfusion
Fig. 12.3 Transvaginal ultrasound scan shows a hyperechoic endometrium due to a decidual reaction, with no chorionic ring in the
uterus. Serum hCG = 914 IU/l.
conditions. We did not find these values in the intrauterine color-
flow signals from ectopic pregnancies. This observation may be
helpful as a differentiating sign.
Clinical examples. Figures 12.3–12.6 illustrate a typical case of
an asymptomatic tubal ectopic pregnancy that was detected
early and managed by a tube-conserving procedure.
Figures 12.
7–12.9 are from a case with a false-positive diag-
nosis caused by a richly vascularized corpus luteum. Multiple,
thorough searches were necessary to find a small intrauterine
chorionic structure signifying an early pregnancy. A history of
irregular cycles with prolonged amenorrhea had caused a
three-week error in dating the pregnancy.
113
Color Doppler Sonography in Ectopic Pregnancy
Fig. 12.4 A chorionic structure is distinguishable from the left ovary
in the left adnexal region.
12
Fig. 12.6 Laparoscopic view of the asymptomatic ectopic pregnancy
(same patient as in Figs. 12.3–12.5) shows a fusiform swelling of the
right tube with no hemoperitoneum or signs of rupture.
Fig. 12.5 Intense color Doppler signals are seen at the periphery of
the extrauterine chorionic structure. The color scale was adjusted to
display low flow velocities (slow-flow imaging). The sampled Doppler
spectrum (triplex mode) shows low indices (PI = 0.7, RI = 0.5, S/D
ratio = 2) characteristic of a low perfusion resistance at the sampled
site. There is a marked similarity to the blood flow patterns of uteroplacental vessels.
Fig. 12.7 Right adnexal mass in a patient with a positive pregnancy
test and an “empty” uterus by transvaginal sonography. The assumed
gestational age is 7 weeks. Color Doppler shows heavy vascularization
with numerous color-flow signals (slow-flow imaging, low signal detection threshold ⬍ 0.028 m/s).
114
Fig. 12.8 Selectively acquired Doppler spectrum indicates low perfu-
sion resistance at the sampled site.
Fig. 12.9 Initially missed intrauterine chorion consistent with the 5th
week of gestation (same patient as in Figs. 12.7 and 12.8).
Assessment of the Method
Little extra effort. It would be an overstatement to claim that
color Doppler vaginal sonography is indispensable for the early
detection of ectopic pregnancy, since an experienced sonographer using quality equipment can diagnose an ectopic pregnancy with reasonable confidence even without color Doppler.
It is known that a radical improvement in diagnostic accuracy
can be achieved only through tremendous effort. Today,
however, the widespread availability of color-flow techniques
gives many examiners the opportunity to increase their diagnostic confidence level with little extra effort, even if only to a
statistically moderate degree. With its protean clinical mani-
Summary
References
festations, it is rare for an ectopic pregnancy to exhibit a typical
course. Color Doppler sonography thus offers a valuable aid to
differential diagnosis.
Triplex mode. There are no compelling, fundamental arguments against the use of color Doppler sonography, but the examiner should be aware of the high energy outputs that are associated with imaging in the triplex mode. Since the uterus
may contain a very early pregnancy that is still below the resolution limit of the ultrasound system, the uterine cavity should
be shielded from triplex scanning to eliminate exposure as a
potential issue. The case in Figs. 12.
portance of this aspect.
7–12.9 illustrates the im-
The introduction of transvaginal sonography has significantly
improved diagnostic accuracy in patients with a suspected ectopic pregnancy. The added use of color Doppler ultrasound
and its capabilities have been addressed and studied by
numerous groups of authors. All have documented a modest
increase in diagnostic efficiency, and our own experience has
confirmed this. The positive predictive value has improved
from approximately 90% to 95 % while the false-positive rate
has decreased from 8.4 % to 5%. A potential source of error is
the corpus luteum, which can have a great diversity of clinical
presentations. For safety reasons, the uterus should not be exposed to prolonged ultrasound scanning in the triplex mode.
The typical candidate for transvaginal color Doppler evaluation has an “empty” uterus and a positive pregnancy test or a
serum hCG level of 1000 IU/l or more with no clinical symptoms. The early detection of ectopic pregnancy helps to reduce
morbidity and increase the prospects for an organ-conserving
laparoscopic procedure.
References
1 Bonilla-Musoles FM, Ballester MJ, TarinJJ, Raga F, Osborne NG, Pellicer
A: Does transvaginal color Doppler sonography differentiate between
developing and involuting ectopic pregnancys? J. Ultrasound Med. 3
(1995) 175
2 De Crespigny LC: Demonstration of ectopic pregnancy by transvaginal
ultrasound. Brit. J. Obstet. Gynaecol. 95 (1988) 1253
3 Emerson DS, Cartier MS, Altieri LA et al.: Diagnostic efficacy of en-
dovaginal color Doppler flow imaging in an ectopic pregnancy screening program. Radiology 183 (1992) 413
4 Kivikosky AI, Martin CM, Smeltzer JS: Transabdominal and transvagi-
nal ultrasonographyin the diagnosis of ectopic pregnancy: a comparative study. Amer. J. Obstet. Gynecol. 163 (1990) 123
5 Kurjak A, Zalud J, Jurkovic D, Alfirevic Z, Miljan M: Transvaginal color
Doppler for the assessment of pelvic circulation. Acta Obstet. Gynecol.
Scand. 68 (1989) 131
6 Meyers M, Feyock A, Holland S, Taylor KJW: Correlation of duplex
Doppler and HCG levels in ectopic pregnancy. Radiology 173 (1989)
247
7 Nyberg DA, Hill LM: Normal early intrauterine pregnancy: sono-
graphic development and hCG correlation. In: Transvaginal ultrasound. Mosby, St. Louis 1992, 65–84
8 Rein MS, Di Salvo DN, Friedman AJ: Heterotopic pregnancy associated
with in vitro fertilization and embryo transfer: possible role for
routine vaginal ultrasound. Fertil. Steril. 51 (1989) 1057
9 Rempen A.: Vaginal sonography in ectopic pregnancy: A prospective
evaluation. J. Ultrasound Med. 7 (1988) 381
10 Salim A, Zalud J, Farmakides G, Schulman H, Kurjak A, Latin V.: Corpus
luteum blood flow in normal and abnormal early pregnancy: evaluation with transvaginal colour and pulsed Doppler sonography. J. Ultrasound Med. 13 (1994) 971
11 Schurz B, Wenzel R, Eppel W, Schon HJ, Reinold E: Early detection of
ectopic pregnancy by transvaginal ultrasound. Arch. Gynecol. Obstet.
248 (1990) 25
12 Taylor KJW, Ramos IM, Feyock AL et al.: Ectopic pregnancy: duplex
Doppler evaluation. Radiology 173 (1989) 93
13 Taylor KJW, Meyer WR: New techniques in the diagnosis of ectopic
pregnancy. Obstet. Gynecol. Clin. N. Am. 18 (1991) 39
14 Voigt HJ: Pathologie der Frühschwangerschaft. Gynäkologe 29 (1996)
165
Obstetric Ultrasound
115
Physiology of Doppler Flow in Maternal Vessels
13
during Pregnancy
T. Golaszewski, J. Deutinger, and G. Bernaschek
Conditions of Intrauterine Life
The introduction of Doppler flow measurements has enhanced
our ability to investigate the conditions of intrauterine fetal
life. For more than 20 years, fetal Doppler ultrasound has provided a simple, noninvasive method for measuring blood flow
velocities in the fetal vessels
uterine blood flow, or the maternal part of the fetomaternal
circulation, were first reported in 1983
Physical Principles
13
Doppler effect. Christian Doppler (born in Salzburg in 1803)
described the effect by which sound waves are perceived as
having a higher or lower frequency, depending on whether the
source of the sound is moving toward or awayfrom the listener.
The amount of this frequency shift is directly related to the
velocity of the sound source. By applying this effect, it was
possible to measure the frequency shift between the ultrasound emitted by a transducer and the echoes returning from
red blood cells and thus determine the velocity of blood flow in
fetal and maternal vessels. We know from hemodynamics that
the blood flow velocity (i.e., the velocity of the moving red
cells) in a vessel is directly proportional to the blood pressure
and indirectly proportional to the vascular resistance.
Continuous-wave transducers. Various types of Doppler transducer are available. Continuous-wave (CW) transducers consist of a transmitter that continuously emits sound and a receiver that continuously receives the frequency-shifted
echoes. One disadvantage of CW Doppler is that it does not discriminate echoes according to their depth. In theory, multiple
vessels along the path of the beam can lead to superimposed
signals and summation effects.
23
. Doppler measurements of
3
.
Since the advent of transvaginal sonography and the
development of color-encoded pulsed Doppler technology,
Doppler flow measurements of the uterine artery and arcuate
arteries have been substantially improved. The color mapping
of blood flow is particularly advantageous for examining the
maternal circulation owing to the many small-caliber vessels
in the maternal system.
Pulsed-wave transducers. Pulsed-wave (PW) transducers emit
ultrasound for a fraction of a second and then switch to the receive mode. These instruments can provide depth discrimination by measuring the echo delay time. Only the echoes that return from a specified tissue depth are analyzed for their
frequency shift. This selected depth, called the Doppler gate or
sample volume, can be positioned precisely within the vessel
lumen, allowing signals to be acquired from a uniquelydefined
anatomical location.
Color Doppler. A color Doppler system displays not only the
magnitude of the frequency shift but also the direction of blood
flow (either towardor away from the transducer) by means of a
color-encoding system (red = toward the transducer, blue =
away from the transducer). This makes it easier to locate small
vessels such as the arcuate arteries.
Indices. Several angle-independent indices can be used to analyze the frequency-shift data: the S/D ratio of Stuart (S = maximum frequency shift in systole, D = minimum frequency shift
in diastole), the resistance index of Pourcelot (RI = (S–D)/S),
and the pulsatility index (PI = (S–D)/mean value).
116
Anatomical and Physiological Principles
Uteroplacental blood supply. The uterus derives most of its
blood supply from the two uterine arteries, which arise from
the iliac artery. A small amount of blood is also supplied by
anastomoses with the ovarian vessels, which branch directly
from the abdominal aorta. The two uterine artery trunks divide
within the myometrium into 10–15 arcade vessels on both
sides. These vessels encircle the uterus and form anastomoses
near the anterior and posterior midline. The radial arteries
arise from these arcade vessels and pass more deeply into the
uterus. The radial arteries in turn give rise to the basal arteries,
which supply the basal endometrium and the spiral arteries
with blood. The tortuous, helixlike spiral arteries supply blood
to the placenta; this blood enters the intervillous space from
the decidua basalis through broad openings in the spiral arteries.
Adaptive Processes during Pregnancy
Spiral arteries. At one time it was believed that the ends of the
spiral arteries bore constrictions that produced a “jet effect.” If
this were true, a high resistance would be present in the spiral
arteries. In fact, invading trophoblasts destroy the muscular
portion of the spiral artery wall within the decidua by the 20th
week of gestation, causing the lumen toexpand in the direction
of the placenta and creating a pressure difference of only
8 mmHg between the spiral artery and the amniotic
Uterine enlargement. Normally the uterus increases greatly in
size during the course of pregnancy. The weight of a gravid
uterus at term is 20 times the uterine weight outside of pregnancy (1000 g versus 50 g). The weight increase is not due
mainly to an increased number of muscle fibers but to muscular hyperplasia, i.e., a marked enlargement of the muscle fibers
of the myometrium. The blood supply during pregnancy
adapts accordingly.
Arterial dilatation. The uterine arteries dilate to approximately
3 times their original caliber, the arcuate arteries to 10 times,
and the spiral arteries to 30 times
15
. By the end of pregnancy,
blood is flowing through the intervillous space at a rate of approximately 60 ml/min
28
. The systemic blood pressure prevails
to the level of the arcuate arteries. Beyond that, the pressure
dwindles to the spiral artery openings, resulting in a low pressure gradient relative to the intervillous space (perfusion pressure 15–20 mmHg).
cavity
25
.
Technique of Transvaginal Pulsed Doppler Flowmetry
It is apparent, then, that Doppler ultrasound scans of the
uterine vessels are representative only to the level of the arcuate arterial bed.
Placental blood supply. Because of the numerous anastomoses
between the two uterine arteries, both vessels supply the
placenta. The uterine arteries each supply a different number
of cotyledons, depending on the placental location, and this accounts for the normal difference between the two sides that is
recorded with Doppler flowmetry.
Perfusion in normal and abnormal pregnancies. In a normal
pregnancy, the maternal uterine arteries reflect the perfusion
of the entire uterofetoplacental circulation. Owing to the tremendous increase in terminal vascular branches, the peripheral flow resistance declines, causing a rise in diastolic flow
velocity. This results in part from progesterone-induced va-
sodilation and from the development of the intervillous space.
In an abnormal pregnancy, vasoconstriction may occur in
the uterine circulation (hypertension, preeclampsia) producing a high S/D ratio, or there may be an inadequate development of collateral channels causing an abnormal discrepancy
between the sides. Normally a postsystolic notch in the Doppler waveform does not persist beyond the 24th week of gestation. If it persists after 24 weeks, the possibility of an impending pregnancy complication should be considered.
The following values are normal for the third trimester:
➤
S/D ratio of the uterine arteries ⬍ 3, difference between the
sides ⬍ 1
➤
S/D ratio of the arcuate arteries ⬍ 2
Obstetric Ultrasound
Technique of Transvaginal Pulsed Doppler Flowmetry
Patient position. In all vaginal ultrasound examinations, it is
advantageous to place the patient in a lithotomy position as
this allows greater mobility of the endovaginal probe. This
position does not compromise uterine blood flow, eliminating
the possibility of false-positive findings
34
.
Transducer placement. Contact gel is applied to the ultrasound
probe, which is then covered with a condom-like sterile rubber
sheath. A lubricating gel is applied, and the probe is carefully
inserted into the vagina. It is oriented to provide a sagittal scan
of the lesser pelvis. A standard routine should be followed for
Doppler flowmetry. In all of our examinations the right side of
the monitor is caudal in the sagittal scan, and the left side is
cranial. The probe is rotated 90⬚ to obtain a coronal or trans-
verse scan, in which case the right side of the monitor corresponds to the patient’s left side, and vice versa
7
.
Adjusting the Doppler beam and sample volume. After making
an initial survey of the lesser pelvis and identifying key landmarks (cervix, gestational sac, ovary, pelvic wall), the examiner
positions the ultrasound probe in the lateral fornix of the
vagina. Rotating the probe 90⬚ makes it easier to locate the
uterine artery in the parametrium, which can be examined in
coronal section. The echogenic parametrium is surveyed by
slowly moving the scanner anteriorly from the sacrum. With
some practice, the uterine artery can be consistently identified
as an elongated, pulsating vascular echo 2–4 mm in diameter.
Besides its typical course, which can be defined over a variable
length, the pulsations of the uterine artery are its most important distinguishing feature.
The examination is done with a minimum amount of probe
pressure. When the vessel has been located in the real-time
scan, the Doppler beam and sample volume are adjusted so
that the Doppler frequency shift can be received and recorded.
It takes from 5 to 10 minutes to examine both uterine arteries
and interpret their spectra. The total examination time depends partly on gestational age.
In late pregnancy it can be difficult or impossible to position
the probe in the lateral fornix owing to the low position of the
presenting fetal part. This is not a problem, however, because
Doppler velocimetry of the uterine arteries is used mainly for
the early detection of pregnancy complications and is rarely
performed after 36 weeks.
117
Physiology of Doppler Flow in Maternal Vessels during Pregnancy
Authors’ Studies
Instruments. We use an end-fire vaginal probe (KretzTechnik,
Zipf, Austria) with a 240⬚ field of view. This instrument can
cover all of the lesser pelvis, making orientation easier. We use
a transducer frequency of 7.5MHz and a Doppler beam
frequency of 4.5 MHz. The optimum pulse repetion frequency
(PRF) setting for most examinations is 5.2 kHz with a penetration depth of approximately 7–8 cm and a 125Hz filter settings. According to the manufacturer, the power output of the
scanner is less than 100 mW/cm
Parameters. In principle, all of the angle-independent parameters mentioned above can be used for waveform analysis.
However, because the maternal vessels exhibit diastolic flow
even when the peripheral resistance is extremely high (early
pregnancy, hypertension), it is sufficient to use simple indices
such as the S/D ratio or RI. The qualitative analysis of Doppler
waveforms would mainly be useful for detecting a postsystolic
notch and has not found wide application
13
Uterine Perfusion in a Normal Pregnancy
Establishing normal values. We performed transvaginal Dopp-
ler velocimetric studies of the uterine artery in singleton pregnancies from 7 to 40 weeks’ gestation in order to establish normal values
for enrollment in the study were an ultrasound examination in
early pregnancy for accurate dating, an uncomplicated course
of pregnancy, and a birthweight within normal limits.
6
. We analyzed the data from 88 women. The criteria
2
.
12, 36
.
pulsatility with high systolic flow velocities and low end-diastolic velocities. The further progression of pregnancy is marked
by an increase in the flow velocities, especially during diastole,
causing a signif icant decrease in the S/D ratio (Fig. 13.
Second and third trimesters. The greatest changes in our study
were observed at the start of the second trimester. We saw no
significant increase in diastolic flow velocity after the end of
the second trimester. The mean S/D ratio was 5.44 in the first
trimester and 2.20 in the third trimester, while the pulsatility
index fell from 2.59 to 1.32 (Figs. 13.
Differences between the sides. When we compared the right
and left uterine arteries by their respective contributions to the
uterine blood supply, we noted some marked differences between the two sides in early pregnancy, which were also responsible for the large scatter of individual values measured in
the first and second trimesters. When the mean values for both
vessels were compared, however, no differences were found.
The difference in the S/D ratio between the right and left
uterine arteries decreased during the third trimester and averaged only 0.4–0.3. In the third trimester of a normal pregnancy,
the S/D ratio in both uterine arteries was less than 3, while the
difference between the sides was less than 1.
3 and 13.4).
2).
118
Early pregnancy. Figure 13.
parametrium demonstrating the uterine artery and a Doppler
waveform pattern that is typical of early pregnancy, i.e., high
Fig. 13.1 Example of an original transvaginal pulsed Doppler scan of
the left uterine artery in the first trimester of pregnancy. Transverse
scan through the uterine wall at the level of the isthmus shows numerous color-encoded vessels of small caliber. The Doppler sample
volume is positioned in the descending branch of the left uterine
artery. The peripheral resistance is still high at this stage, and consequently the diastolic flow velocities are low.
1 shows a coronal scan through the
Fig. 13.2 Transabdominal Doppler velocimetry of the right uterine
artery in the second trimester of pregnancy. The high flow velocity in
diastole is caused by the low peripheral resistance, which is considered
a sign of adequate placentation and uterine blood flow.
Authors’ Studies
9
8
7
S/D-ratio
6
5
4
3
2
1
0
5–8
9–12
17– 20
13–16
21–24
25–28
29–32
Weeks of gestation
37–40
33–36
4.5
4.0
3.5
3.0
Pulsatility index
2.5
2.0
1.5
1.0
0.5
0
5–8
9–12
17– 20
13–16
21–24
25–28
29–32
Weeks of gestation
37–40
33–36
Fig. 13.3 Fall of the S/D ratio during the course of pregnancy. Fig. 13.4 Fall of the pulsatility index during the course of pregnancy.
patients (64%), the S/D ratios and left–right differences were
Uterine Perfusion in an Abnormal Pregnancy
within our normal values. These cases served as the control
group (group I). In 63 patients (36%) we found values that were
In another study, uterine artery Doppler velocimetry was performed in 176 women with singleton pregnancies (114 primi-
outside our normal range. These patients were subdivided into
five groups (II–VI) with abnormal uterine perfusion (Fig. 13.
5).
parae and 62 multiparae) between the 27th and 40th weeks of
gestation
reasons:
➤
Suspected fetal growth retardation (94)
➤
Risk history (30)
➤
Pregnancy-induced hypertension (23)
➤
Diabetes mellitus (16)
➤
Chronic hypertension (13)
8
.
The women were enrolled in the study for the following
Fetal circulation. The results of Doppler flow measurements in
fetal arteries were grouped in relation to uterine perfusion and
compared with the control group. We found that most cases
with abnormal flow velocities in fetal vessels belonged to
groups III, V and VI. In groups III and VI, all of the fetuses had an
abnormal waveform in one of the three vessels examined
(umbilical artery, aorta, internal carotid artery). Most of the fetuses in group V (35 of 38) had an abnormal flow velocity in at
least one of the vessels examined (Table 13.
2).
S/D ratio and PI. The S/D ratio was used for waveform analysis.
Three parameters were used for the classification of uterine
perfusion, drawing on our tables of normal values: the S/D
ratio in the right uterine artery, the S/D ratio in the left uterine
artery, and the left–right difference. Analysis of the fetal circulation was based on the S/D ratio and the pulsatility index (PI)
of the umbilical artery, aorta, and internal carotid artery. For
further analysis we classified the calculated values as normal
or abnormal by referring to published normal values (S/D ratio
in the umbilical artery ⬍ 3
of the internal carotid artery ⬎ 1.3
31
; PI of the fetal aorta ⬍ 2.237; and PI
40
).
Obstetric Ultrasound
Six groups of uterineperfusion. We were able to distinguish six
different groups of uterine perfusion based on the calculated
S/D ratios and left–right differences in the uterine arteries
(Table 13.
1). They were distributed as follows: in 113 of the 176
Table 13.1 Definition of groups I–VI in relation to uterine perfusion
Left-right difference ⬍ 1 ⬎ 1
Both S/D ratios ⬍ 3
One S/D ratio ⬎ 3
Both S/D ratios ⬎ 3
I
II
III
IV
V
VI
Fig. 13.5 Transvaginal pulsed Doppler scan of the left uterine artery
in the 25th week of gestation, showing an elevated S/D ratio. The
waveform also contains a postsystolic notch. In this case the preg-
nancy was complicated by preeclampsia.
119
Physiology of Doppler Flow in Maternal Vessels during Pregnancy
Table 13.2 Normal and abnormal Doppler waveforms (n = number of
patients) of fetal vessels in relation to uterine perfusion (groups I–VI)
Group I II III IV V VI
n 113 10 4 5 38 6
Normal ratios in all
fetal vessels
%344004080
Abnormal 74 6 4 3 35 6
% 66 60 100 60 92 100
UA + aorta + ICA – – 2 – – –
UA + aorta 15 2 1 – 13 2
UA + ICA – 1 – – 3 –
Aorta + ICA 3 – – 1 – 1
UA 14 3 – – 5 –
Aorta 34 – 1 1 12 3
ICA 8 – – 1 2 –
UA = umbilical artery, ICA = internal carotid artery
Uterine Perfusion on Medication or following
13
Uterine Manipulation
39 4 0 2 3 0
Table 13.3 Demographic data on the patients examined
Group 1 Group 2 Group 3 Group 4
Medication None Oral None i.v.
Surgical pro-
cedure
n 30 30 28 29
Age (years)
⫾ SD
Primiparae 6 4 9 10
Multiparae 24 26 19 19
Amniocentesis
37.8 ⫾ 2.3 38.2 ⫾ 2.4 26.4
Amniocentesis
Cerclage Cerclage
⫾ 2.5
25.1
⫾ 2.9
Doppler velocimetry. Transvaginal Doppler velocimetry was
performed before and after surgery or medication between the
14th and 16th weeks of pregnancy. In groups 1 and 2 we performed Doppler flowmetry before and 24 hours after amniocentesis. In groups 3 and 4 the measurements were taken
before and six hours after cervical cerclage. We analyzed the
mean values of both measurements and then evaluated the
total perfusion of the uterus. We based our analysis on the S/D
ratio, pulsatility index, and maternal heart rate.
We also did a study to determine how amniocentesis, cervical
cerclage, or the administration of beta-mimetics would affect
uterine blood flow
9
.
Results. The diastolic blood flow velocity rose significantly
after cervical cerclage and the postoperative administration of
i.v. beta-mimetics. This was caused mainly by a fall in periph-
eral resistance. This phenomenon was observed only in group
Six groups. We examined a homogeneous population of 117
women (Table 13.
3) who were randomly divided into four
groups. Groups 1 and 2 consisted of women who underwent
genetic amniocentesis for advanced maternal age. These
patients either received no beta-mimetics (group 1) or prophylactic oral beta-mimetics (group2). Groups 3 and 4 consisted of
women who underwent prophylactic cervical cerclage. Group
3 did not receive i.v. beta-mimetic prophylaxis, while group 4
did. Further clinical data on the patients are presented in Table
13.
3. The oral beta-mimetics were administered in six in-
4. Amniocentesis (group 1) and cerclage alone (group 3) had no
effect on uterine perfusion. Oral treatment with beta-mimetics
(group 2) also caused no change in uterine perfusion. In the
patients who received i.v. beta-mimetics (group 4), we found a
significant decrease in the S/D ratio and pulsatility index of the
uterine arteries and a rise in the maternal heart rate. Thus, only
the i.v. administration of beta-mimetics led to an increased
perfusion rate of the pregnant uterus in the second trimester
(Table 13.
4).
dividual doses of 10mg each. The i.v. beta-mimetics were administered at a rate of 0.2 mg/min.
Table 13.4 Hemodynamic parameters of uterine perfusion before and after surgery and/or prophylactic beta-mimetics
Group 1 Group 2 Group 3 Group 4
Medication None Oral None i.v.
Surgical procedure Amniocentesis Amniocentesis Cerclage Cerclage
120
S/D preoperative 2.63 ⫾ 0.70 2.67 ⫾ 0.90 2.62 ⫾ 1.14 2.69 ⫾ 1.1 7
S/D postoperative 2.66 ⫾ 0.76 2.54 ⫾ 0.86 2.61 ⫾ 0.76 2.11 ⫾ 0.44*
PI preoperative 1.53 ⫾ 0.44 1.67 ⫾ 0.46 1.54 ⫾ 0.46 1.62 ⫾ 0.47
PI postoperative 1.54 ⫾ 0.40 1.58 ⫾ 0.75 1.50 ⫾ 0.48 1.21 ⫾ 0.30*
HR preoperative 85.3 ⫾ 11.6 81.4 ⫾ 11.4 84.0 ⫾ 12.6 82.6 ⫾ 11.1
HR postoperative 90.2 ⫾ 13.2 89.7 ⫾ 18.5 83.9 ⫾ 15.9 99.4 ⫾ 15.7*
S/D = S/D ratio; PI = pulsatility index; HR = maternal heart rate
* p ⬍ 0.05
Discussion
Uterine Perfusion in a Normal Pregnancy
Early Pregnancy
Arcuate arteries. Methods of flowmetry on the maternalside of
the fetomaternal circulation continue to be controversial. Two
decades ago, Campbell et al.
the flow pattern of the arcuate arteries could be recorded much
earlier than with any other known parameters
mal, early decline in the resistance and pulsatility indices of
the radial and spiral arteries that can be detected in the first
trimester with color Doppler sonography
this method are its poor reproducibility, uncertainty over the
precise anatomical source of the measurement, and the fact
that each uterine artery divides into 12–15 arcuate arteries.
The shape of the waveforms depends on whether the measure-
ments are taken on the inside or outside of the uterine wall.
Also, the pulsatility index depends on the maternal heart rate
and is therefore highly variable. The best parameters for Doppler flow analysis at the level of this vascular bed are the S/D
ratio and the resiatnce index
detectable between 17and 20 weeks’ gestation at the center of
the placenta, where the RI and PI are significantly lower than at
the periphery
22
.
The increase in uterine blood flow has been correlated with
the size of the conceptus, underscoring the importance of the
physiology of uterine perfusion in the first trimester. Uterine
blood flow shows a linear increase up until the 9th weekof gestation, and thereafter it rises exponentially
sonography during the first trimester can already show a
difference of uterine blood flow in patients with a threatened
abortion or molar pregnancy compared with women with a
normal pregnancy
18, 2 0
Uterine arteries. The physiological changes in early pregnancy
chiefly affect the uterine vessels and are a result of trophoblastic invasion and enlarged vessel lumina, whereas rheological
factors such as decreased maternal blood viscosity are of no
importance
26
. It has long been known that preeclampsia can
develop owing to deficient trophoblastic invasion and transformation of the spiral arteries into a low-pressure system
Thus, screening for later pregnancy complications can be done
during the first trimester by checking for an abnormal PI in the
uterine arteries
19, 27
.
Reports on transabdominal uterine artery sampling illustrate the difficulty of this type of flowmetry.In many cases it
is not possible to define the uterine artery in the B-mode im-
16
age
. The vaginal approach eliminates a source of error in
these measurements owing to the proximity of the sampled
vessel and appears to be superior to transabdominal scanning.
The transvaginal scanning of both uterine arteries can be done
successfully in early pregnancy and provides a simple method
of examination that is well accepted by patients who have received the necessary information.
Compared with velocimetry of the arcuatearteries, Doppler
sonographyof the uterine arteries permits a more general eval-
3
were able to show that changes in
3
. There is a nor-
24
. Disadvantages of
5
. Spiral arteries are consistently
10
. Color Doppler
.
Discussion
uation of uterine perfusion since the uterine arteries represent
the sum of the flow conditions in all the arcuate arteries. This is
particularly advantageous in patients with extensive placental
infarctions and in smokers. Doppler flowmetry that is confined
to a single, circumscribed area of the placental bed can lead to
erroneous results in some circumstances.
Late Pregnancy
So far, the Doppler velocimetry of maternal vessels has not
yielded convincing results in terms of fetal surveillance
is unlikely from a physiological standpoint, because uterine
artery velocimetry tends to be unrewarding unless there is absent or deficient trophoblastic invasion of the spiral arteries.
The assessment of fetal condition at term or the detection of
fetal compromise is accomplished more effectively with fetal
heart rate monitoring
35
.
Uterine Perfusion in an Abnormal Pregnancy
Fetal growth retardation and/or pregnancy-induced hypertension. Abnormal waveformsin the uterine vessels show a strong
correlation with the presence or subsequent development of
fetal growth retardation and preeclampsia
values in the uterine artery show a significantly higher association with premature delivery and low birthweight compared
with normal flow patterns
30
.
In our study of high-risk pregnancies, we examined one
group of patients with normal uterine perfusion and five
groups with varying degrees of abnormal uterine perfusion. In
cases with pregnancy-induced hypertension or fetal growth
retardation, many of the spiral arteries are left out of the transformation into a low-impedance vascular bed or are resistant
to such a change. This is manifested by an increase in the S/D
ratio by Doppler flowmetry. It is our opinion that group VI had
the most severe degree of abnormal uterine perfusion. All of
the fetuses in that group responded to the deficient blood
supply with abnormal flow velocities in at least one vessel.
One abnormal perfusion parameter. The mildest form of ab-
4
.
normal uterine perfusion appears to exist when only one parameter (the S/D ratio in one uterine artery or a difference b etween the right and left sides) is abnormal. Hemodynamically,
we can interpret this finding as follows: only one uterine artery
has undergone normal expansion and transformation into a
low-impedance vessel with high diastolic flow, while the contralateral artery has not undergone this change or has failed to
form normal collateral channels. This type of pathology appears to have only a moderate adverse effect on the fetal circulation, however. Apparently there has been adequate fetal cardiovascular compensation for the decrease in uterine perfusion.
Two or three abnormal perfusion parameters. When two or
three parameters of uterine perfusion were abnormal (increased S/D ratio in one or both uterine arteries, with or
33
. Abnormal PI
13
. This
Obstetric Ultrasound
121