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66 Teisala K, Heinonen PK, Punnonen R: Transvaginal ultrasound in the
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67 Thurmond AS, Patton PE, Hector DM, Jones MK: US-guided fallopian
tube catherization. Radiology 180 (1991) 571–572
68 Thurmond A, Rosch J: Nonsurgical fallopian tube recanalization for
treatment of infertility. Radiology 174 (1990) 371–374
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fallopian tube. Obstet. Gynecol. 70 (1987) 424–428
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humans by in vitro fertilization and embryo transfer in the controlled
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tubal patency by transvaginal sonosalipingography. Fertil. Steril. 57
(1992) 336–340
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(TSSG) in the evaluation of tubal patency. Acta Eur. Fertil. 22 (1991)
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sonographic tubal patency testing air and saline solution as contrast
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Transvaginal ovarian cyst puncture in the early follicular phase of an
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Infertility Evaluation and Assisted Reproduction
93
Obstetric Ultrasound
Doppler Ultrasound Examinations from Folliculogenesis
10
to Early Pregnancy
S. Kupesic, A. Kurjak, and W. Schmidt
Overview
The introduction of transvaginal color Doppler sonography has
dramatically enhanced our understanding of early human
development. This study permits the noninvasive assessment
of blood flow in the corpus luteum and the changes in uterine
blood flow that occur in association with pregnancy. For example, when corpus luteum blood flow was analyzed in normal and abnormal pregnancies, no difference was found between ectopic pregnancy and normal early pregnancy, but the
resistance and pulsatility indices in cases of threatened abortion, incomplete abortion, and missed abortion were found to
10
be significantly higher than in normal pregnancies.
In several studies, color Doppler imaging has shown a progressive decline in the resistance and pulsatility indices from
the main branch of the uterine artery to the spiral arteries with
advancing gestational age. All the vessels examined showed a
decrease in flow resistance as the pregnancy progressed.
Transvaginal color Doppler ultrasound has provided a
unique opportunity to study both the morphology and physiology of human life from conception to implantation. The
follicular cells become luteinized after ovulation. Many biochemical, morphological, and circulatory changes take place
during this transformation process, and a large proportion of
these changes can be investigated by transvaginal color Doppler scanning. After fertilization of the oocyte, the embryo is
transported into the uterine cavity, where it implants under
favorable local and hormonal conditions and develops into a
new individual. Transvaginal ultrasound with color Doppler
imaging and blood flow analysis during these phases permits a
detailed examination of the small vessels that supply the preovulatory follicle, corpus luteum, and endometrium.
96
Monitoring Folliculogenesis
The ovary and ovarian blood flow. Transvaginal ultrasound
scanning also permits an increasingly precise visualization of
ovarian morphology
sound makes it easier to measure the sequential changes in the
arteries that supply the ovaries during the course of the cy-
2, 3, 4, 24, 38
cle
first day of the cycle, the lowest on the day of the LH (luteinizing hormone) peak
Follicular blood flow. The surveillance of folliculogenesis with
ultrasound has become a well-established modality in routine
clinical practice. The blood flow at the periphery of the follicle
can be clearly demonstrated with transvaginal color Doppler
ultrasound
can be recorded when the dominant follicle has reached a
diameter of 10 mm. The resistance index (RI) is approximately
0.54 in the periovulatory period
decline two days before ovulation and reaches its lowest value
when ovulation occurs (0.44 ⫾ 0.04). Measurements taken
shortly before ovulation typically show a sharp rise in the peak
systolic blood flow velocity with a relatively constant resistance index. This observation may result from dilatation of
the newly formed vessels between the vascularized theca cell
layer and the hypoxic granulosa cell layer of the follicle
mal ovulation depends upon changes in the oxygen partial
pressure and the effect of these changes on cellular function
. The highest flow resistance is measured on the
3, 4
. Normally, a follicular flow velocity waveform
8
. The addition of color Doppler ultra-
3, 4
.
24
(Fig. 10.1). The RI begins to
12
. Nor-
Fig. 10.1 Transvaginal scan of the dominant follicle three days before
ovulation indicates a moderate vascular resistance (RI = 0.65). Color
Doppler ultrasound can define the small vessels that supply the follicle.
(Fig. 10.
ing is b ecoming the method of choice for investigating the subtle blood flow changes that take place in the normally and abnormally functioning ovary (Fig. 10.
2). Transvaginal sonography with color Doppler imag-
3).
Development of the Corpus luteum
Fig. 10.2 Triangular outline of the mature follicle. Fig. 10.3 Image of an ovary with numerous follicles after prior ovula-
tion induction with hCG. Each follicle is ringed by vascular structures
that can be visualized with Doppler ultrasound.
Development of the Corpus luteum
Developmental stages. The cells of the follicular wall undergo
structural and functional changes as they develop into the
components of the corpus luteum
pus luteum undergoes four developmental stages: proliferation (Fig. 10.
4), vascularization, maturation, and regression. In
the proliferative phase, the theca interna becomes infolded
while its vascular channels become greatly dilated. Vessels
sprout from the endothelium, penetrate the granulosa cell
layer, and enter the hemorrhagic cavity of the ruptured follicle.
The vascularization phase is characterized by a rapid organization of the blood-filled cavity of the ruptured follicle (Figs. 10.
10.
6). With increasing maturation, the theca cells and the
lutein cells derived from the granulosa acquire vacuoles and
are physiologicallyactive. The mature corpus luteum measures
1–3 cm in section and displays low resistance signals (average
RI = 0.43). Regressive changes in the corpus luteum can be seen
as early as day 23 of the cycle (Fig.10.
changes are marked by a decreased blood flow velocity and a
17
. Microscopically, the cor-
7). Typically these
5,
Fig. 10.4 Early development of the corpus luteum in a transvaginal
color Doppler scan. Note the dilated vessels at the periphery of the collapsed follicle (left). A decreased vascular resistance (RI = 0.40) is demonstrated (right).
Obstetric Ultrasound
Fig. 10.5 Transvaginal power Doppler image showing increased
vascularization of the corpus luteum.
Fig. 10.6 Typical blood flow pattern of the mature corpus luteum:
high blood flow velocity and low vascular resistance (RI = 0.47).
97
Doppler Ultrasound Examinations from Folliculogenesis to Early Pregnancy
rising resistance index (average RI =0.49). If pregnancy occurs,
the corpus luteum persists in response to hCG (human
chorionic gonadotropin) synthesized by the trophoblasts and
produces progesterone to support the developing embryo. The
corpus luteum begins to regress after 10 weeks’ gestation, at
which time the placenta assumes the task of progesterone production. Regression of the corpus luteum is complete by the
16th week of gestation
The use of Doppler ultrasound during these stages can
supply interesting information
assessment of blood flow velocity in the corpus luteum provides direct information on the arterial perfusion of the
26, 32
ovary
small vessels in the ovary. The results are very precise and re-
Fig. 10.7 Transvaginal scan of the ovary in the late luteal phase (left).
During the luteal regression phase, diastolic blood flow is decreased
and the RI is increased (right).
producible.
Changes in Endometrial Blood Flow
29
.
15, 36
. The noninvasive Doppler
. Transvaginal color Doppler can demonstrate even
10
Uterine blood supply. Implantation and subsequent pregnancy
in humans are dependent upon complexchanges in the uterine
artery and its branches in the myometrium and endometrium.
The blood flow changes in the uterine vessels during a reproductive cycle are important for implantation and for the
development of a uteroplacental blood supply. Transvaginal
color Doppler gives a detailed view of the genital organs and of
most blood flow changes that occur in these organs
color-flow signal from the uterine artery can be identified
lateral to the cervix (Fig. 10.
third of the myometrium, the uterine arteries divide into the
vascular plexus of the arcuate arteries, which are distributed
within the uterus
18
. The radial arteries arise from this plexus
and run toward the uterine cavity (Fig. 10.
junction of the myometrium and endometrium, they are called
the spiral arteries. Transvaginal color Doppler is an efficient
8). After passing through the outer
9). On reaching the
19
. The
tool for analyzing the waveforms of the radial and spiral arteries.
It is well known that the endometrium undergoes profound
structural and functional changes during the course of the cy-
9, 11, 18, 33
cle
. Demonstrable histological changes include the
vigorous development of essential blood vessels, especially the
spiral arteries, during the menstrual cycle (Fig. 10.
10). The in-
creased blood flow to the endometrium depends on blood flow
changes that occur in the uterine arteries, in the arcuate
plexus, and in the radial arteries.
Blood flow changes in the uterine arteries. Complex relationships appear to exist between the levels of circulating ovarian
hormones in the peripheral venous blood and uterine blood
flow
parameters
13, 27
. In most women, low end-diastolic blood
flow is measured in the uterine arteries during the proliferative
98
Fig. 10.8 Scan of the uterine artery lateral to the cervix at the level of
the corpus–cervix junction (left). The end-diastolic flow velocity in the
uterine artery is decreased before ovulation, with RI = 0.87 (right).
Fig. 10.9 The radial arteries can be clearly visualized with Doppler ultrasound.
Fig. 10.10 The detection of color-flow signals from the spiral arteries
at the periphery of the hyperechoic endometrium during the luteal
phase is suggestive of normal uterine receptivity.
phase29. The resistance index of the uterine arteries during this
phase is 0.88 ⫾ 0.04 and begins to fall on the day before ovulation. In a normal ovulatory menstrual cycle, the end-diastolic
blood flow velocity shows a sharp rise between the proliferative and secretory phases. The lowest resistance index
(RI = 0.84 ⫾ 0.04) is measured on day 18 of the cycle, and this
remains constant until the end of the cycle. Because the
changes in blood flow velocity begin before ovulation, it is reasonable to assume that they are related both to angiogenesis
and to hormonal factors. Some authors have noted the absence
of end-diastolic flow in the uterine arteries of infertility
patients and have related it to low fertility or infertil-
13,14,29, 35
ity
disappears with the onset of pregnancy
. However, this finding could also be a variant that
29
. The changes de-
scribed above cannot be demonstrated in anovulatory cycles.
Changes in Endometrial Blood Flow
Blood flow changes in the radial and spiral arteries. With trans-
vaginal color Doppler sonography, it is possible to investigate
blood flow changes that occur in the radial and spiral arteries
under normal and abnormal conditions. A fall in the resistance
and pulsatility indices across the uterine artery toward the spiral arteries can be detected in the uterus of nonpregnant
women. The RI in the radial arteries during the proliferative
phase is 0.78 ⫾ 0.10. This index begins to fall significantly at
midcycle and reaches its lowest value in the midluteal phase
(0.68 ⫾ 0.04). The RI in the spiral arteries is 0.54 ⫾ 0.03 on the
day before ovulation (Fig. 10.
(0.49 ⫾ 0.05) approximately between days 16 and 18 of the
cycle (Fig. 10.
12). The changes in the blood flow parameters of
the radial and spiral arteries correspond to the blood flow
changes that are measured in the uterine arteries.
Therapeutic implications. Transvaginal color Doppler sonography appears to provide a means of predicting implantation
rates, investigating previously unexplained infertility problems, and referring patients with impaired myometrial and endometrial blood flow for appropriate therapy. Another logical
application of this technique is in testing the effects of various
medications on uterine blood flow
changes in endometrial blood flow could play an important
role in determining the optimum timing for implantation and
embryo transfer. In this regard, transvaginal color Doppler can
provide a tool for the noninvasive assessment of uterine receptivity. This will enable clinicians to cryopreserve embryos
when uterine conditions are poor and transfer a smaller number of embryos when the conditions are optimal (Figs. 10.
10.
14).
11) and reaches its lowest value
21
. A knowledge of the
13,
Obstetric Ultrasound
Fig. 10.11 Spiral artery waveform in the periovulatory phase. The low
RI (0.50) and increased blood flow velocity are characteristic of ovula-
tion.
Fig. 10.12 Transvaginal scan demonstrates a thickened endometrium. The color areas represent the spiral arteries (left). Analysis of
the pulsed Doppler spectrum (right) shows a low to moderate vascular
resistance, which is characteristic of normal endometrial receptivity.
99
Doppler Ultrasound Examinations from Folliculogenesis to Early Pregnancy
Fig. 10.13 Uterine artery waveform in an infertile patient (left). Note
the absence of diastolic blood flow (RI = 1.0) (right).
Fig. 10.14 Absent diastolic flow in the uterine artery on the predicted day of ovulation (right). This finding may occur in association
with low fertility or infertility.
Luteal Blood Flow in Normal and Abnormal Pregnancies
10
A total of 181 pregnancies were studied: 127 with a normal course
of pregnancy and 54 with an abnormal course. The course of pregnancy in both groups was routinely evaluated with ultrasound. All of
the patients had regular cycles before their pregnancy.
Material and methods. The uterus, gestational sac, embryo, and
ovaries were examined with transvaginal B-mode ultrasound. The
pulsed Doppler signals were acquired in a 2 mm wide sample
volume using the Aloka color Doppler SSD-680 and 2000 systems
(Aloka Corporation, Tokyo, Japan) with a 5 MHz transducer. Blood
flows were recorded in 90⬚ sectors at a scanning depth of 2–20 cm.
The pulse repetition frequency was between 2 and 32 kHz, and
100Hz wall filters were used to eliminate unwanted low-frequency
signals. The maximum energy density was 80 mW/cm
below the FDA-prescribed limit for fetal ultrasound. The waveforms
of all the sampled vessels were determined twice by each examiner.
Three different cardiac cycles were recorded in each run, and the RI
was computed. The average length of the examination was less
than 20 minutes.
Results. None of the 127 women in the uncomplicated pregnancy
group had an RI higher than 0.5 in the 5th– 12th week of gestation.
The resistance and pulsatility indices showed no statistically signifi-
blood flow after 12 weeks is attributed to regression of the luteal
vessels. Studies of the intraovarian blood supply raise the question
whether there are factors other than hCG that sustain corpus lu-
teum function
women is negative and is of no significance, luteal blood flow is
present throughout the second half of the cycle. Kratzer et al.
found that corpus luteum function in early pregnancy was dependent on the rate of the hCG increase. The authors also found that this
rate of increase was lower in patients with ectopic pregnancy and
spontaneous abortion than in women with a normal course of pregnancy. The resistance and pulsatility indices during the luteal phase
1,5, 10, 34, 37
. Although the hCG value in nonpregnant
2
, which is
Implications. It appears that luteal blood flow has prognostic
significance in cases of threatened abortion. An elevated RI
suggests a decreased chance of embryo survival, especially
after eight weeks’ gestation, when the critical period for survival is concluded. It seems reasonable to use luteal blood flow
as a parameter for corpus luteum regression that can be correlated with other regulatory factors such as progesterone, relaxin, prostaglandin, and angiogenetic peptide growth hormone. Prostaglandin F
produced locally by luteal cells during the regression phase.
Because PGF
resistance in the corpus luteum vessels (reflected in the RI or
20
PI). It remains unclear whether endothelial-derived relaxing
factor (EDRF) also plays a role. It is also unclear whether vascular factors are important in luteal phase disturbances. Transvaginal scanning and pulsed Doppler sonography will certainly
be of help in the further investigation of these questions.
follow the same pattern in patients with ectopic pregnancy as in
nonpregnant women
responds to that in normal early pregnancy (p ⬎ 0.05). Luteal blood
flow during the first trimester of pregnancy is comparable to that in
a nonpregnant woman during the luteal phase. In cases of inevi-
table abortion, imminent abortion or missed abortion, the resistance and pulsatility indices are significantly increased relative to
the normal population (p ⬍ 0.001). Zalud and Kurjak
luteal blood flow in the ovary of nonpregnant women and in ectopic
and intrauterine pregnancies. The RI of luteal blood flow was lowest
in the nonpregnant women (0.42 ⫾ 0.12) and highest in the women
with an intrauterine pregnancy (0.53 ⫾ 0.09). The RI in ectopic
pregnancies was 0.48 ⫾ 0.07. Luteal blood flow was present on the
affected side in 86.4 % of the ectopic pregnancies.
2α
32
. Luteal blood flow in ectopic pregnancy cor-
38
investigated
(PGF2α), also known as luteolysin28,is
2α
is a potent vasoconstrictor, it can increase the
100
Trophoblastic Invasion and Development of the Placenta
References
Trophoblastic invasion. After the blastocyst has established
contact with the endometrium, the trophoblast penetrates
deep into the endometrium and first encounters dilated
venous vessels, followed by superficial arterioles and finally, in
the 4th week of gestation, the spiral arteries
18, 19
. Cytotrophoblastic cells reach the boundary between the decidua and myometrium between the 8th and 12th weeks of gestation
31
. The
trophoblastic invasion of the myometrium continues until the
18th week
7
. The spiral arteries undergo a morphological transformation in early pregnancy as the trophoblast partially disrupts the vascular structure, causing hypertrophy of the
smooth-muscle cells of the media and thickening of the endothelium
7, 30
.
Blood flow changes. The erosion of the spiral arteries and altered steroid hormone levels in the plasma cause a significant
fall of uterine vascular resistance. It is common to detect low
vascular resistance and turbulence, especially near the placen-
22
ta
. Jaffe and Warsof16observed Doppler waveform changes in
connection with placentation as early as the 5th week of gestation.
Kurjak et al.
23
described the occurrence of Doppler changes
in early pregnancy even before a gestational sac could be identified. These changes consist of low peak systolic flow velocities in the periphery of the endometrium. Larger maternal vessels are eroded as the placenta continues to develop, with
Doppler ultrasound showing higher blood flow velocities with
an increased diastolic component.
Outlook. The uteroplacental vascular supply and blood flow
during pregnancy have been the subject of extensive re-
6, 25
search
. Color Doppler sonography, as an adjunct to trans-
vaginal B-mode imaging, is broadening our knowledge of the
functional aspects of fetal morphology and physiology. Normal
development of the embryo depends upon chromosomal
structure, implantation mechanism, and uterine perfusion.
Poor implantation conditions and a deficient blood supply can
be detected noninvasively by Doppler scanning. In the future,
transvaginal color Doppler sonography could become the procedure of choice in threatened abortion cases for differentiating among the various causes of abnormal hemodynamic
changes.
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