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DOPPLER ULTRASOUND IN OBSTETRICS

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Author(s): Alfred Abuhamad, MD
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The Doppler effect, which was first reported by Christian Doppler in 1842 [1,2] , describes
the apparent variation in frequency of a light or a sound wave as the source of the wave
approaches or moves away, relative to an observer. The traditional example that is given to
describe this physical phenomenon is the apparent change in sound level of a train as the
train approaches and then departs a station. The sound seems higher in pitch as the train
approaches the station and seems lower in pitch as the train departs the station. This
apparent change in sound pitch, or what is termed the frequency shift, is proportional to the
speed of movement of the sound-emitting source. In clinical applications, when ultrasound
with a certain frequency (fo) is used to insonate a certain blood vessel, the reflected
frequency (fd) or frequency shift is directly proportional to the speed with which the red
blood cells are moving (blood flow velocity) within that particular vessel. This frequency
shift of the returning signal is displayed in a graphic form as a time-dependent plot. In this
display, the vertical axis represents the frequency shift and the horizontal axis represents the
temporal change of this frequency shift as it relays to the events of the cardiac cycle [Fig.
1] . This frequency shift is highest during systole, when the blood flow is at its fastest, and
lowest during end- diastole, when the blood flow is at its slowest in the peripheral
circulation. Given that the velocity of flow in a particular vascular bed is inversely
proportional to the downstream impedance to flow, the frequency shift therefore derives
information on the downstream impedance to flow of the vascular bed under study. The
frequency shift is also dependent on the cosine of the angle that the ultrasound beam makes
with the targeted blood vessel [see formula in Fig. 1 ]. Given that the insonating angle is
difficult to measure in clinical practice,indices that rely on ratios of frequency shifts were
developed to quantitate Doppler waveforms. By relying on ratios of frequency shifts, these
Doppler indices are thus independent of the effects of the insonating angle of the ultrasound
beam. Doppler indices that are commonly used in obstetrical practice are shown in Fig. 2 .

FETAL ARTERIAL DOPPLER

Umbilical arterial circulation

The umbilical arterial circulation is normally a low impedance circulation [Fig. 3] , with
an increase in the amount of end diastolic flow with advancing gestation [3,4]. Umbilical
arterial Doppler waveforms reflect the status of the placental circulation, and the increase in
end diastolic flow that is seen with advancing gestation is a direct result of an increase in
the number of tertiary stem villi that takes place with placental maturation [5,6] . Diseases
that obliterate small muscular arteries in placental tertiary stem villi result in a progressive
decrease in end-diastolic flow in the umbilical arterial Doppler waveforms until absent, and
then reverse flow during diastole is noted [Fig. 4] [7,8] . Reversed diastolic flow in the
umbilical arterial circulation represents an advanced stage of placental compromise, and is
associated with more than seventy percent of placental arterial obliteration[912]. The
presence of absent or reversed end diastolic flow in the umbilical artery is commonly
associated with severe intrauterine growth restriction and oligohydramnios [13,14].

Doppler waveforms of the umbilical arteries can be obtained from any segment along the
umbilical cord. Waveforms obtained from the placental end of the cord show more end
diastolic flow than waveforms obtained from the abdominal cord insertion [15,16].
Differences in Doppler indices of arterial waveforms obtained from different anatomic
locations of the same umbilical cord are generally minor and have no significance on
clinical practice [3,4].

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.

Middle cerebral circulation

The cerebral circulation is normally a high impedance circulation with continuous forward flow
throughout the cardiac cycle [Fig. 5] [17,18]. The middle cerebral artery is the most accessible
cerebral vessel to ultrasound imaging in the fetus, and it carries more than 80% of cerebral
blood flow [19,20]. In the presence of fetal hypoxemia, central redistribution of blood flow
occurs, resulting in an increased blood flow to the brain, heart, and adrenals,and a reduction in
flow to the peripheral and placental circulations. This blood flow redistribution is known as the
brain-sparing reflex, and plays a major role in fetal adaptation to oxygen deprivation [Fig.
6] [17,2022].

The right and left middle cerebral arteries represent major branches of the circle of Willis in the
fetal brain. The circle of Willis, which is supplied by the internal carotids and vertebral arteries,
can be imaged with color flow Doppler ultrasound in a transverse plane of the fetal head
obtained at the base of the skull [Fig. 7] . In this transverse plane, the proximal and distal
middle cerebral arteries are seen in their longitudinal view, with their course almost parallel to
the ultrasound beam [see Fig. 7 ]. Middle cerebral artery Doppler waveforms, obtained from
the proximal portion of the vessel, immediately after its origin from the circle of Willis, have
shown the best reproducibility [18,23].

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

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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.

Fetal venous Doppler

Doppler waveforms obtained from the central venous circulation in the fetus reflect the
physiologic status of the right ventricle. Specific information with regards to right ventricular
preload, myocardial compliance, and right ventricular end-diastolic pressure can be derived from
Doppler flow studies of the inferior vena cava and ductus venosus in the fetus [2433].

Inferior vena cava Doppler waveforms can be obtained from a coronal plane of the chest and
abdomen. In this view, the inferior vena cava can be imaged as it enters into the right atrium,
joined by the ductus venosus and the left hepatic vein [Fig. 8] . The inferior vena cava can be
studied at two locations: at the inlet into the right atrium, or in the segment between the
entrance of the renal vein and the ductus venosus. A good correlation coefficient exists between
these two measurement sites, and the location that provides the smallest angle of insonation
with the blood flow should be chosen [25,31]. Inferior vena cava Doppler waveforms are
triphasic in shape, with the first phase corresponding to ventricular systole, the second phase to
early diastole, and the third phase to late diastole or the atrial kick [Fig. 9].

Ductus venosus Doppler waveforms can be easily obtained from a transverse view of the fetal
abdomen at the same anatomic plane of the abdominal circumference. By superimposing color
flow Doppler to the gray-scale image, the ductus venosus can be identified as it branches from
the umbilical vein[Fig. 10]. Turbulence is commonly seen within the ductus venosus given its
narrow lumen [see Figs. 9,10 ]. The presence of turbulence on color flow Doppler helps in
identifying the ductus venosus in early gestations. Ductus venosus Doppler waveforms are
biphasic in shape, with the first phase corresponding to ventricular systole, the second phase to
early diastole, and the nadir of the second phase to late diastole or the atrial kick [Fig. 11].

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

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Fig. 5
Middle cerebral artery Doppler waveforms in a
normal fetus in the third trimester of
pregnancy. Note the high-impedance circulation
with decreased end diastolic velocity.

Fig. 6
Middle cerebral artery Doppler waveforms in a
growth-restricted fetus showing a low-
impedance circulation with an increase in the
end-diastolic velocity.

Fig. 7
Color Doppler at the base of the fetal brain
showing the circle of Willis. MCA, middle
cerebral artery.
FETAL CARDIAC DOPPLER

Doppler indices in fetal echocardiography are quantitative parameters, and are for the majority,
angle dependent. To obtain accurate Doppler indices in fetal echocardiography, the sample
volume is placed distal to the respective valves, the insonating angle should be within 15 to 20
of the direction of blood flow, Doppler waveforms should be obtained during fetal apnea, and
multiple measurements should be made. Color Doppler is used to direct placement of the
sample volume; placing the sample volume at the brightest colors of the blood flow segment will
ensure the best measurements. Fig. 12 shows Doppler indices commonly used in fetal
echocardiography.

The fetal circulation is different from the adult circulation in many aspects. The fetal circulation
is in parallel, rather than in series, and the right ventricular cardiac output is greater than the
left ventricular cardiac output [6,7,34,35]. The progressive development of organs during
gestation influences blood distribution and vascular impedance[6,34]. With advancing gestation,
ventricular compliance is increased, total peripheral resistance is decreased, preload is
increased, and combined cardiac output is increased [6,34]. Compliance of the fetal left heart
increases more rapidly than compliance compliance of the fetal right heart with advancing
gestation [6,34]. The pulmonary vascular resistance is high in the fetus and the pulmonary
arterial pressure is almost systemic[9,10,32,36]. Flow to the pulmonary vascular bed is
maintained at a low rate with a noted increase toward the end of gestation [7,9,32,35]. Cardiac
output in the fetus is mainly affected by preload and ventricular compliance [6,34]. The
presence of right to left shunts at the level of the foramen ovale and ductus arteriosus has a
significant impact on cardiac flow patterns and affects the distribution of blood and oxygen to
various organs. Flow across the foramen ovale contributes to the majority of blood entering the
left ventricle and more than two thirds of right ventricular output is directed to the ductus
arteriosus[7,13,35,37]. This shunting mechanism ensures the delivery of blood with high
oxygen content to the coronary and cerebral circulations.

Fig. 8
Coronal view of the fetal chest and abdomen
with color Doppler showing the ductus
venosus (DV)and the hepatic vein (superior
to the ductus venosus)joining the inferior
vena cava (IVC) before it enters the right
atrium.
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Fig. 9
Doppler velocity waveforms of the inferior
vena cava in a normal fetus in the third
trimester of pregnancy. See text for details.

Fig. 10
Transverse plane of the fetal abdomen at the
level of the abdominal circumference. Color
Doppler ultrasound shows the ductus
venosus (arrow) as it branches from the
umbilical vein.

Doppler waveforms across the atrioventricular valves are bicuspid in shape. The first peak (E
wave), corresponds to early ventricular filling of diastole, and the second peak (A wave)
corresponds 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 ventricular 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].
Fig. 11
Doppler velocity waveforms of the ductus venosus in a
normal fetus in the third trimester of pregnancy. See
text for details.

Doppler waveforms across the semilunar valves are uniphasic in shape. Indices most commonly
used for the semilunar Doppler waveforms include the peak systolic velocity (PSV) and the time
to peak velocity (TPV). PSV and TPV increase with advancing gestation across the semilunar
valves[2,3,5,6,8,13,19,21,23,33,34,37]. PSV is higher across the aorta than across the
pulmonary artery because of a decreased afterload and a smaller diameter across the
aorta [2,3,5,6,8,13,19,21,23,33,34,37]. These Doppler indices reflect ventricular
contractility, arterial pressures, and afterloads.

FETAL DOPPLER AND INTRAUTERINE GROWTH RESTRICTION

Arterial Doppler abnormalities, at the level of the umbilical and middle cerebral arteries (brain-
sparing reflex), confirm the presence of hypoxemia in the growth-restricted fetus, and present
early warning signs. Once arterial centralization occurs, however, no clear trend is noted in the
observational period, and thus arterial redistribution may not be helpful for the timing of the
delivery [11,12,14,4042]. On the other hand, the presence of reversed diastolic flow in the
umbilical arteries is a sign of advanced fetal compromise, and strong consideration should be
given for delivery, except for extreme prematurity. Cesarean section should be given preference
in this setting, because labor may cause further fetal compromise.

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.

The current literature suggests that venous Doppler abnormalities in the inferior vena cava and
ductus venosus and abnormal fetal heart rate monitoring, even in its computerized version,
follow arterial Doppler abnormalities and are thus associated with a more advanced stage of fetal
compromise[16,18,20,22,3639,43,44].
Furthermore, in the majority of severely growth-restricted fetuses, sequential deterioration of
arterial and venous Doppler precedes biophysical profile score deterioration [22,37]. At least
one third of fetuses show early signs of circulatory deregulation 1 week before biophysical rofile
deterioration,and that in most cases, Doppler deterioration preceded biophysical profile
deterioration by 1 day [22,37].
The occurrence of such abnormal late stage changes of vascular adaptation by the intrauterine
growth-retarded (IUGR) fetus appears to be the best predictor of perinatal death, independent of
gestational age and weight [39,43]. In a longitudinal study on Doppler and IUGR fetuses, all
intrauterine deaths and all neonatal deaths, with the exception of one case, had late Doppler
changes at the time of delivery, whereas only a few of the surviving fetuses showed such
changes [39,43].

This sequential deterioration of the hypoxemic,growth-restricted fetus is rarely seen at

gestations beyond 34 weeks [18,45,46]. Indeed, normal umbilical artery Doppler is common in
growth-restricted fetuses in late gestations, and cerebroplacental ratios have poor correlation
with outcome of IUGR fetuses at greater than 34 weeks of gestation [35,47]. Caution should
therefore be exercised when Doppler is used in the clinical management of IUGR fetuses beyond
34 weeks of gestation.

The pathophysiology of fetal growth restriction has not been fully described because recent
studies have highlighted the presence of significant variation in fetal adaptation to hypoxemia.
The pattern of incremental deterioration of arterial Doppler abnormalities, followed by venous
Doppler abnormalities,then followed by fetal heart tracings and biophysical profile abnormalities,
is not seen in about 20% of preterm fetuses [16,36]. Furthermore, only 70% of IUGR fetuses
show significant deterioration of all vascular beds by the time they were delivered, and about
10% showed no significant circulatory change by delivery time [22,37]. In a prospective,
observational study, more than 50% of IUGR fetuses delivered because of abnormal fetal heart
rate tracings did not have venous Doppler abnormalities [39]. In view of these findings, the
universal introduction of venous Doppler in the clinical management of the growth-restricted
fetus should await the results of randomized trials on this subject.

IUGR is associated with several changes at the level of the fetal heart involving preload,
afterload, ventricular compliance, and myocardial contractility. An increase in afterload is seen
at the level of the right ventricle because of increased placental impedance [25,48]. A
decrease in afterload is noted at the level of the left ventricle because of decreased cerebral
impedance associated with the brain-sparing reflex [25,48]. These changes in afterload result
in a redistribution of the cardiac output from right to left ventricle [25,48]. Preload is reduced
at both atrioventricular valves because of hypovolemia and decreased filling associated with
IUGR [21,24,26,30,31,45,49,50]. This decrease in preload is reflected by a decrease in
the E/A ratio, decreased atrial peak, and decreased time velocity integral at the mitral and
tricuspid valves [21,24,26, 45,49,50].
Evidence of reduced myocardial contractility in the presence of severe IUGR has also been
reported. Ventricular ejection force, an index of ventricular systolic function that is independent
of preload and afterload is decreased at the level of the right and left ventricle in fetal growth
restriction [31,36]. IUGR fetuses that have reduced ventricular ejection force have a shorter
time to delivery, a higher incidence of nonreassuring fetal heart rate tracing, and a lower pH at
birth when compared with controls [31,36]. A significant correlation between the severity of
fetal acidosis at cordocentesis and ventricular ejection force values validates the association of
this index and the severity of fetal compromise [31,36]. Myocardial cell damage,
demonstrated by elevated levels of cardiac troponin-T, is seen in some fetuses that have severe
growth restriction [25,28]. This advanced stage of fetal compromise is associated with signs
of increased systemic venous pressure, a change in the distribution of cardiac output, a rise in
right ventricle afterload, and a high incidence of tricuspid regurgitation [25,28]. These
findings suggest that Doppler abnormalities in the proximal venous system of the growth
restricted fetus suggest fetal myocardial cell damage and increased systemic venous
pressure[25,28].

The fetal heart plays a central role in the adaptive mechanisms for hypoxemia and placental
insufficiency. As discussed in this article, longitudinal data on the hemodynamic sequence of the
natural history of fetal growth restriction show that the umbilical artery and middle cerebral
artery are the first variables to become abnormal [27,34]. These arterial Doppler
abnormalities are followed by abnormalities in the right cardiac diastolic indices, followed by the
right cardiac systolic indices, and finally by both left diastolic and systolic cardiac
indices [27,34]. Preserving the left systolic function as the last variable to become abnormal
ensures an adequate left ventricular output, which supplies the cerebral and coronary
circulations.
Several of the Doppler changes seen in association with fetal IUGR in the peripheral circulation
are directly related to the adaptation of the fetal heart. The current management of IUGR
involves Doppler at the peripheral arterial circulation (middle cerebral and umbilical arteries),
central venous vessels (ductus venosus and inferior vena cava), and cardiotocography. Adding
cardiac Doppler may improve management of the IUGR fetus, but studies are lacking on the
prospective clinical evaluation of the IUGR fetus with cardiac Doppler. It is becoming more
obvious, however, that those changes in the central venous circulation reflect an advanced stage
of fetal compromise, commonly associated with myocardial dysfunction and damage.