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293

ULTRASOUND
CLINICS

Ultrasound Clin 1 (2006) 293–301

Doppler Ultrasound in Obstetrics


Alfred Abuhamad, MD

& Fetal arterial Doppler & Fetal cardiac Doppler


Umbilical arterial circulation & Fetal Doppler and intrauterine growth
Middle cerebral circulation restriction
Fetal venous Doppler & References

The Doppler effect, which was first reported by portional to the downstream impedance to flow,
Christian Doppler in 1842 [1,2], describes the ap- the frequency shift therefore derives information
parent variation in frequency of a light or a sound on the downstream impedance to flow of the vas-
wave as the source of the wave approaches or cular bed under study. The frequency shift is also
moves away, relative to an observer. The traditional dependent on the cosine of the angle that the
example that is given to describe this physical phe- ultrasound beam makes with the targeted blood
nomenon is the apparent change in sound level of vessel [see formula in Fig. 1]. Given that the inso-
a train as the train approaches and then departs a nating angle is difficult to measure in clinical prac-
station. The sound seems higher in pitch as the tice, indices that rely on ratios of frequency shifts
train approaches the station and seems lower in were developed to quantitate Doppler waveforms.
pitch as the train departs the station. This apparent By relying on ratios of frequency shifts, these Dopp-
change in sound pitch, or what is termed the fre- ler indices are thus independent of the effects of
quency shift, is proportional to the speed of move- the insonating angle of the ultrasound beam. Dopp-
ment of the sound-emitting source. In clinical ler indices that are commonly used in obstetrical
applications, when ultrasound with a certain fre- practice are shown in Fig. 2.
quency (fo) is used to insonate a certain blood
vessel, the reflected frequency (fd) or frequency
shift is directly proportional to the speed with Fetal arterial Doppler
which the red blood cells are moving (blood flow
velocity) within that particular vessel. This fre- Umbilical arterial circulation
quency shift of the returning signal is displayed in The umbilical arterial circulation is normally a low-
a graphic form as a time-dependent plot. In this impedance circulation [Fig. 3] , with an increase in
display, the vertical axis represents the frequency the amount of end diastolic flow with advancing
shift and the horizontal axis represents the tem- gestation [3,4]. Umbilical arterial Doppler wave-
poral change of this frequency shift as it relays to forms reflect the status of the placental circulation,
the events of the cardiac cycle [Fig. 1]. This fre- and the increase in end diastolic flow that is seen
quency shift is highest during systole, when the with advancing gestation is a direct result of an in-
blood flow is at its fastest, and lowest during end- crease in the number of tertiary stem villi that takes
diastole, when the blood flow is at its slowest in the place with placental maturation [5,6]. Diseases that
peripheral circulation. Given that the velocity of obliterate small muscular arteries in placental ter-
flow in a particular vascular bed is inversely pro- tiary stem villi result in a progressive decrease in

Department of Obstetrics and Gynecology, Eastern Virginia Medical School, Hofheimer Hall, Suite 310,
8254 Fairfax Avenue, Norfolk, VA 23507, USA
E-mail address: abuhamaz@evms.edu

1556-858X/06/$ – see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.cult.2005.12.001
ultrasound.theclinics.com
294 Abuhamad

Fig. 1. The Doppler effect (fd) is dependent on the velocity of flow (V ) of the blood within a vessel, the initial
frequency of the ultrasound beam (fc), and the cosine of the angle (A) that the ultrasound beam makes with the
direction of flow. The Doppler effect is displayed on the monitor as a time-dependent plot of the frequency shift
(fd) within a cardiac cycle.

end-diastolic flow in the umbilical arterial Doppler waveforms obtained from the abdominal cord
waveforms until absent, and then reverse flow insertion [15,16]. Differences in Doppler indices
during diastole is noted [Fig. 4] [7,8]. Reversed of arterial waveforms obtained from different ana-
diastolic flow in the umbilical arterial circulation tomic locations of the same umbilical cord are
represents an advanced stage of placental compro- generally minor and have no significance on clin-
mise, and is associated with more than seventy ical practice [3,4].
percent of placental arterial obliteration [9–12].
The presence of absent or reversed end diastolic Middle cerebral circulation
flow in the umbilical artery is commonly associated The cerebral circulation is normally a high-
with severe intrauterine growth restriction and impedance circulation with continuous forward
oligohydramnios [13,14]. flow throughout the cardiac cycle [Fig. 5] [17,18].
Doppler waveforms of the umbilical arteries can The middle cerebral artery is the most accessible
be obtained from any segment along the umbilical cerebral vessel to ultrasound imaging in the fetus,
cord. Waveforms obtained from the placental end and it carries more than 80% of cerebral blood flow
of the cord show more end diastolic flow than [19,20]. In the presence of fetal hypoxemia, central

Fig. 2. Doppler indices that are commonly used in obstetrics. D, diastole; PI, pulsatility index; RI, resistive index;
S, systole.
Doppler Ultrasound in Obstetrics 295

Fig. 3. Umbilical artery Doppler waveforms in a normal fetus in the third trimester of pregnancy. Note the low-
impedance circulation with increased end-diastolic velocity.

redistribution of blood flow occurs, resulting in an Fetal venous Doppler


increased blood flow to the brain, heart, and adre- Doppler waveforms obtained from the central
nals, and a reduction in flow to the peripheral and venous circulation in the fetus reflect the physiolo-
placental circulations. This blood flow redistribu- gic status of the right ventricle. Specific information
tion is known as the brain-sparing reflex, and plays with regards to right ventricular preload, myocar-
a major role in fetal adaptation to oxygen depriva- dial compliance, and right ventricular end-diastolic
tion [Fig. 6] [17,20–22]. pressure can be derived from Doppler flow studies
The right and left middle cerebral arteries repre- of the inferior vena cava and ductus venosus in the
sent major branches of the circle of Willis in the fetus [24–33].
fetal brain. The circle of Willis, which is supplied by Inferior vena cava Doppler waveforms can be
the internal carotids and vertebral arteries, can be obtained from a coronal plane of the chest and
imaged with color flow Doppler ultrasound in a abdomen. In this view, the inferior vena cava can
transverse plane of the fetal head obtained at the be imaged as it enters into the right atrium, joined
base of the skull [Fig. 7]. In this transverse plane, by the ductus venosus and the left hepatic vein
the proximal and distal middle cerebral arteries are [Fig. 8]. The inferior vena cava can be studied at
seen in their longitudinal view, with their course two locations: at the inlet into the right atrium, or
almost parallel to the ultrasound beam [see Fig. 7]. in the segment between the entrance of the renal
Middle cerebral artery Doppler waveforms, ob- vein and the ductus venosus. A good correlation
tained from the proximal portion of the vessel, coefficient exists between these two measurement
immediately after its origin from the circle of Willis, sites, and the location that provides the smallest
have shown the best reproducibility [18,23]. angle of insonation with the blood flow should be

Fig. 4. Umbilical artery Doppler waveform in a severely growth restricted fetus showing abnormal Doppler
waveforms with reversed diastolic flow.
296 Abuhamad

Fig. 7. Color Doppler at the base of the fetal


brain showing the circle of Willis. MCA, middle cere-
bral artery.

ler to the gray-scale image, the ductus venosus can


be identified as it branches from the umbilical vein
Fig. 5. Middle cerebral artery Doppler waveforms in a
normal fetus in the third trimester of pregnancy. Note [Fig. 10]. Turbulence is commonly seen within the
the high-impedance circulation with decreased end- ductus venosus given its narrow lumen [see Figs. 9,
diastolic velocity. 10]. The presence of turbulence on color flow
Doppler helps in identifying the ductus venosus
chosen [25,31]. Inferior vena cava Doppler wave- in early gestations. Ductus venosus Doppler wave-
forms are triphasic in shape, with the first phase forms are biphasic in shape, with the first phase
corresponding to ventricular systole, the second corresponding to ventricular systole, the second
phase to early diastole, and the third phase to late phase to early diastole, and the nadir of the second
diastole or the atrial kick [Fig. 9]. phase to late diastole or the atrial kick [Fig. 11].
Ductus venosus Doppler waveforms can be easily
obtained from a transverse view of the fetal abdo-
men at the same anatomic plane of the abdominal Fetal cardiac Doppler
circumference. By superimposing color flow Dopp-
Doppler indices in fetal echocardiography are
quantitative parameters, and are for the majority,
angle dependent. To obtain accurate Doppler in-
dices in fetal echocardiography, the sample volume
is placed distal to the respective valves, the insonat-

Fig. 8. Coronal view of the fetal chest and abdomen


with color Doppler showing the ductus venosus (DV)
Fig. 6. Middle cerebral artery Doppler waveforms in a and the hepatic vein (superior to the ductus venosus)
growth-restricted fetus showing a low-impedance cir- joining the inferior vena cava (IVC) before it enters
culation with an increase in the end-diastolic velocity. the right atrium.
Doppler Ultrasound in Obstetrics 297

Fig. 9. Doppler velocity waveforms of the inferior vena cava in a normal fetus in the third trimester of pregnancy.
See text for details.

ing angle should be within 15° to 20° of the direc- ance of the fetal right heart with advancing gesta-
tion of blood flow, Doppler waveforms should be tion [6,34]. The pulmonary vascular resistance is
obtained during fetal apnea, and multiple measure- high in the fetus and the pulmonary arterial pres-
ments should be made. Color Doppler is used to sure is almost systemic [9,10,32,36]. Flow to the
direct placement of the sample volume; placing the pulmonary vascular bed is maintained at a low rate
sample volume at the brightest colors of the blood with a noted increase toward the end of gestation
flow segment will ensure the best measurements. [7,9,32,35]. Cardiac output in the fetus is mainly
Fig. 12 shows Doppler indices commonly used in affected by preload and ventricular compliance
fetal echocardiography. [6,34]. The presence of right to left shunts at the
The fetal circulation is different from the adult level of the foramen ovale and ductus arteriosus has
circulation in many aspects. The fetal circulation is a significant impact on cardiac flow patterns and
in parallel, rather than in series, and the right affects the distribution of blood and oxygen to
ventricular cardiac output is greater than the left various organs. Flow across the foramen ovale con-
ventricular cardiac output [6,7,34,35]. The progres- tributes to the majority of blood entering the left
sive development of organs during gestation influ- ventricle and more than two thirds of right ven-
ences blood distribution and vascular impedance tricular output is directed to the ductus arteriosus
[6,34]. With advancing gestation, ventricular com- [7,13,35,37]. This shunting mechanism ensures
pliance is increased, total peripheral resistance is the delivery of blood with high oxygen content to
decreased, preload is increased, and combined car- the coronary and cerebral circulations.
diac output is increased [6,34]. Compliance of the Doppler waveforms across the atrioventricular
fetal left heart increases more rapidly than compli- valves are bicuspid in shape. The first peak
(E wave), corresponds to early ventricular filling
of diastole, and the second peak (A wave) corre-
sponds to atrial systole or the atrial kick. Unlike in
postnatal life, the velocity of the A wave is higher
than that of the E wave in the fetus [6,15,34,38].
This highlights the importance of the role that atrial
systole plays in cardiac filling in the fetus. E/A ratio
increases with advancing gestation and reflects ven-
tricular diastolic function [6,15,34,38]. E and A
velocity peaks are higher in the right ventricle,
and this right ventricular dominance is noted
from the first trimester [6,15,17,34,38,39]. Shifting
to left ventricular dominance starts in utero toward
the end of gestation [6,34]. E/A ratio is an index of
ventricular preload and compliance [6,34].
Doppler waveforms across the semilunar valves
Fig. 10. Transverse plane of the fetal abdomen at the are uniphasic in shape. Indices most commonly
level of the abdominal circumference. Color Doppler used for the semilunar Doppler waveforms include
ultrasound shows the ductus venosus (arrow) as it the peak systolic velocity (PSV) and the time to
branches from the umbilical vein. peak velocity (TPV). PSV and TPV increase with
298 Abuhamad

Fig. 11. Doppler velocity waveforms of the ductus venosus in a normal fetus in the third trimester of pregnancy.
See text for details.

advancing gestation across the semilunar valves 40–42]. On the other hand, the presence of re-
[2,3,5,6,8,13,19,21,23,33,34,37]. PSV is higher versed diastolic flow in the umbilical arteries is a
across the aorta than across the pulmonary artery sign of advanced fetal compromise, and strong con-
because of a decreased afterload and a smaller sideration should be given for delivery, except for
diameter across the aorta [2,3,5,6,8,13,19,21,23, extreme prematurity. Cesarean section should be
33,34,37]. These Doppler indices reflect ventricular given preference in this setting, because labor may
contractility, arterial pressures, and afterloads. cause further fetal compromise.
The current literature suggests that venous Dopp-
ler abnormalities in the inferior vena cava and
Fetal Doppler and intrauterine growth
ductus venosus and abnormal fetal heart rate moni-
restriction
toring, even in its computerized version, follow
Arterial Doppler abnormalities, at the level of the arterial Doppler abnormalities and are thus asso-
umbilical and middle cerebral arteries (brain-spar- ciated with a more advanced stage of fetal compro-
ing reflex), confirm the presence of hypoxemia in mise [16,18,20,22,36–39,43,44].
the growth-restricted fetus, and present early warn- Furthermore, in the majority of severely growth-
ing signs. Once arterial centralization occurs, how- restricted fetuses, sequential deterioration of ar-
ever, no clear trend is noted in the observational terial and venous Doppler precedes biophysical
period, and thus arterial redistribution may not be profile score deterioration [22,37]. At least one third
helpful for the timing of the delivery [11,12,14, of fetuses show early signs of circulatory deregula-

Fig. 12. Doppler indices that are commonly used in fetal echocardiography. (A) Peak systolic velocity (PSV) is the
peak velocity achieved during one cardiac cycle. (B) Acceleration time (AT) is the time it takes the velocity to reach
its peak in one cardiac cycle. (C ) Time velocity integral (TVI) is the integral of the planimetric area under the curve.
TVI expresses the distance that the red blood cells would have to cover with a constant area of the flow section.
Doppler Ultrasound in Obstetrics 299

tion 1 week before biophysical profile deteriora- hypovolemia and decreased filling associated with
tion, and that in most cases, Doppler deterioration IUGR [21,24,26,30,31,45,49,50]. This decrease in
preceded biophysical profile deterioration by 1 day preload is reflected by a decrease in the E/A ratio,
[22,37]. decreased atrial peak, and decreased time velocity
The occurrence of such abnormal late stage integral at the mitral and tricuspid valves [21,24,26,
changes of vascular adaptation by the intrauterine 45,49,50].
growth-retarded (IUGR) fetus appears to be the Evidence of reduced myocardial contractility in
best predictor of perinatal death, independent of the presence of severe IUGR has also been reported.
gestational age and weight [39,43]. In a longitudi- Ventricular ejection force, an index of ventricular
nal study on Doppler and IUGR fetuses, all intra- systolic function that is independent of preload and
uterine deaths and all neonatal deaths, with the afterload is decreased at the level of the right and
exception of one case, had late Doppler changes left ventricle in fetal growth restriction [31,36].
at the time of delivery, whereas only a few of the IUGR fetuses that have reduced ventricular ejec-
surviving fetuses showed such changes [39,43]. tion force have a shorter time to delivery, a higher
This sequential deterioration of the hypoxemic, incidence of nonreassuring fetal heart rate tracing,
growth-restricted fetus is rarely seen at gestations and a lower pH at birth when compared with con-
beyond 34 weeks [18,45,46]. Indeed, normal trols [31,36]. A significant correlation between the
umbilical artery Doppler is common in growth- severity of fetal acidosis at cordocentesis and ven-
restricted fetuses in late gestations, and cerebropla- tricular ejection force values validates the asso-
cental ratios have poor correlation with outcome of ciation of this index and the severity of fetal
IUGR fetuses at greater than 34 weeks of gestation compromise [31,36]. Myocardial cell damage, dem-
[35,47]. Caution should therefore be exercised onstrated by elevated levels of cardiac troponin-T,
when Doppler is used in the clinical management is seen in some fetuses that have severe growth
of IUGR fetuses beyond 34 weeks of gestation. restriction [25,28]. This advanced stage of fetal
The pathophysiology of fetal growth restriction compromise is associated with signs of increased
has not been fully described because recent studies systemic venous pressure, a change in the distri-
have highlighted the presence of significant varia- bution of cardiac output, a rise in right ventricle
tion in fetal adaptation to hypoxemia. The pattern afterload, and a high incidence of tricuspid regur-
of incremental deterioration of arterial Doppler gitation [25,28]. These findings suggest that Dopp-
abnormalities, followed by venous Doppler abnor- ler abnormalities in the proximal venous system
malities, then followed by fetal heart tracings and of the growth restricted fetus suggest fetal myo-
biophysical profile abnormalities, is not seen in cardial cell damage and increased systemic venous
about 20% of preterm fetuses [16,36]. Further- pressure [25,28].
more, only 70% of IUGR fetuses show significant The fetal heart plays a central role in the adaptive
deterioration of all vascular beds by the time they mechanisms for hypoxemia and placental insuffi-
were delivered, and about 10% showed no signifi- ciency. As discussed in this article, longitudinal
cant circulatory change by delivery time [22,37]. In data on the hemodynamic sequence of the natural
a prospective, observational study, more than 50% history of fetal growth restriction show that the
of IUGR fetuses delivered because of abnormal fetal umbilical artery and middle cerebral artery are the
heart rate tracings did not have venous Doppler first variables to become abnormal [27,34]. These
abnormalities [39]. In view of these findings, the arterial Doppler abnormalities are followed by
universal introduction of venous Doppler in the abnormalities in the right cardiac diastolic indices,
clinical management of the growth-restricted fetus followed by the right cardiac systolic indices, and
should await the results of randomized trials on finally by both left diastolic and systolic cardiac
this subject. indices [27,34]. Preserving the left systolic function
IUGR is associated with several changes at the as the last variable to become abnormal ensures an
level of the fetal heart involving preload, afterload, adequate left ventricular output, which supplies the
ventricular compliance, and myocardial contracti- cerebral and coronary circulations.
lity. An increase in afterload is seen at the level of Several of the Doppler changes seen in asso-
the right ventricle because of increased placental ciation with fetal IUGR in the peripheral circula-
impedance [25,48]. A decrease in afterload is tion are directly related to the adaptation of the
noted at the level of the left ventricle because of fetal heart. The current management of IUGR
decreased cerebral impedance associated with the involves Doppler at the peripheral arterial circula-
brain-sparing reflex [25,48]. These changes in after- tion (middle cerebral and umbilical arteries), cen-
load result in a redistribution of the cardiac output tral venous vessels (ductus venosus and inferior
from right to left ventricle [25,48]. Preload is re- vena cava), and cardiotocography. Adding cardiac
duced at both atrioventricular valves because of Doppler may improve management of the IUGR
300 Abuhamad

fetus, but studies are lacking on the prospective weight neonates with intrauterine growth restric-
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