Acta Obstet Gynecol Scand 1998; 77: 614619

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Copyright C Acta Obstet Gynecol Scand 1998

Acta Obstetricia et
Gynecologica Scandinavica
ISSN 0001-6349

ORIGINAL ARTICLE

Uterine and umbilical artery velocimetry in

pre-eclampsia
KRISTEL VAN ASSELT, SAEMUNDUR GUDMUNDSSON, PELLE LINDQVIST AND KAREL MARSAL
From the Department of Obstetrics and Gynecology, University of Lund, University Hospital MAS, Malmo, Sweden

Acta Obstet Gynecol Scand 1998: 77: 614619. C Acta Obstet Gynecol Scand 1998
Background. The aim of the present study was to evaluate whether Doppler velocimetry of
the placental circulation can predict adverse outcome of pregnancies complicated by preeclampsia and whether there is a correlation between maternal blood pressure, proteinuria
and placental vascular resistance.
Material and methods. One hundred and eight pregnant women with pre-eclampsia were followed and examined by Doppler velocimetry of the uterine arteries. The presence of a notch
and the mean pulsatility index (PI) in the two arteries were recorded. The velocity waveforms
in umbilical arteries were also evaluated. The Doppler velocimetry results were related to the
perinatal outcome, maternal blood pressure and proteinuria.
Results. Abnormal arterial blood velocity waveforms on both sides of the placenta were
significantly correlated with a shorter gestational age at delivery, lower birthweight, increased
cesarean section rate and more frequent admissions to the neonatal intensive care unit. Bilateral rather than unilateral uterine artery notches were predictive of poor perinatal outcome.
The combination of umbilical and uterine artery waveform results was the best predictor of
adverse outcome. The uterine artery velocimetry was, however, not related to maternal blood
pressure or the degree of proteinuria.
Conclusions. Abnormal velocity waveforms in the uterine and umbilical arteries have clinical
significance in pregnancies complicated by pre-eclampsia and predict adverse outcome of
pregnancy, especially the fetal growth restriction and need for operative interventions during
labor and delivery.
Key words: Doppler velocimetry; notch; perinatal outcome; pre-eclampsia; pulsatility index:
umbilical artery; uterine artery
Submitted 28 October, 1997
Accepted 6 December, 1997

Approximately 810% of pregnancies in primigravidas are complicated by pre-eclampsia or pregnancy induced hypertension (PIH), with increased
maternal and perinatal mortality and morbidity
(13). The etiology of pre-eclampsia is still not
completely known. Several theories have been proposed concerning for example possible genetic susceptibility (4), and an imbalance of prostacyclin
and tromboxane (5). There is an indication that
Abbreviations:
PI: pulsatility index: NICU: neonatal intensive care unit; SGA:
small for gestational age newborns; MAP: mean blood
pressure.
C Acta Obstet Gynecol Scand 77 (1998)

the maternal immune system plays an important

role (6). Several patho-physiological mechanisms
were described, the main underlying abnormality
being general vasoconstriction and increased vascular sensitivity to pressor peptides and amines.
Vasoconstriction leads to hypertension, especially
to elevated diastolic blood pressure. Tissue damage
occurs as a consequence of the vasoconstriction
and the activation of coagulation system in several
organs, e.g. the kidneys and liver. Proteinuria
might be a marker of tissue damage (7).
The uteroplacental blood flow increases tenfold
during pregnancy (8, 9). This increase in blood
flow is facilitated by dilatation of the uteroplacen-

Doppler velocimetry in pre-eclampsia

tal vessels (10). One of the main features of preeclampsia is an abnormal placentation by inadequate trophoblastic invasion of the maternal
spiral arteries. The dilatation of the spiral arteries
is therefore halted and blood flow supply reduced
(11, 12).
Doppler examination makes it possible to record
non-invasively the blood flow velocity waveforms
(FVW) of the uterine and umbilical arteries. The
Doppler method has been found clinically useful
in predicting adverse outcome of pregnancy in
high-risk pregnancies, especially in cases of suspected intra-uterine growth retardation (14, 15).
An early diastolic notch in the uterine artery blood
velocity waveform is typical for an increased uteroplacental vascular resistance, but can be a physiological finding before 26 weeks of gestation (13).
The aim of the present study was to evaluate
whether Doppler velocimetry of the placental circulation could predict adverse outcome in pregnancies complicated by pre-eclampsia and to investigate whether a correlation exists between maternal blood pressure, proteinuria and increased
placental vascular resistance.
Material and methods

A total of 108 pregnant women were enrolled in

this study. All women were referred to the Doppler
ultrasound laboratory for fetal evaluation because
of pre-eclampsia which was defined as: severe preeclampsia (systolic blood pressure 160 mmHg
and diastolic 110 mmHg and/or proteinuria of
3 (3.0 g/L) (Redia-test, Boehringer Mannheim
GmbH, Mannheim, Germany)) or mild pre-eclampsia (systolic blood pressure 145155 mmHg
and diastolic 90 to 105 mmHg and proteinuria 1
or 2 (0.3 and 3.0 g/L). Eighty out of 108
women had mild pre-eclampsia and twenty-eight
severe pre-eclampsia. All women had a singleton
pregnancy.
Blood pressure and proteinuria were measured
at the same time as the last Doppler ultrasound
examination before delivery. The mean blood
pressure (MAP) was defined as systolic blood
pressure 2 diastolic blood pressure/3. Gestational
age was ascertained in all patients by routine ultrasound examination at 18 weeks of pregnancy. The
placenta location was determined during the routine ultrasound examination at 32 weeks of gestation and was classified as either mainly unilateral
or central including fundal, anterior and posterior.
Doppler examinations were performed with an
Acuson 128 XP duplex scanner with pulsed and
color Doppler options using 3.5 MHz transducer
and 125 Hz high-pass filter. Recordings from the
umbilical artery were obtained from a free-floating

615

central part of the cord during absence of fetal

breathing and body movements. Both uterine arteries were located by color Doppler imaging and
the sample volume placed in the vessels cranial to
the crossing of the iliac arteries.
The obtained blood velocity waveforms were
analyzed for Pulsatility Index (PI) according to
Gosling et al. (16). Three subsequent heart cycles
were analyzed and PI values were related to normal reference values for umbilical and uterine arteries (15, 17). Mean PI of both uterine arteries
1.20 was considered abnormal. Abnormal umbilical artery PI values were those above the mean
2 s.d. for gestational age.
The results of the last examination before delivery were correlated to perinatal outcome characterized by gestational age at birth, birthweight,
birthweight deviation in percent from the mean of
the normal population, placental weight, mode of
delivery, Apgar score at 1 and 5 min of life, incidence of admission to the neonatal intensive care
unit (NICU) as well as umbilical cord arterial and
venous blood pH. Small for gestational age (SGA)
newborns were defined as a birthweight below
mean 2 s.d. of the Scandinavian population (18).
Fishers exact test, Students t-test and odds
ratio with confidence interval were used for statistical analysis, p0.05 being regarded as significant. Spearman rank correlation coefficient was
used for the analysis of relationship between the
degree of proteinuria and uterine artery PI and
mean arterial pressure.
Results

Patient characteristics according to the type of preeclampsia are given in Table I. Although the uterTable I. Patient characteristics and results of Doppler velocimetry. Median
(range), numbers or percentages are given
Type of pre-eclampsia
Severe
Number
Gestational age at the last
examination (weeks) (range)
Primiparity
Placenta location
unilateral
central
Uterine artery notch
absent
bilateral
unilateral
Abnormal uterine artery PI
(1.20)
Abnormal umbilical artery PI
(mean2 s.d.)

Mild

p value

28
80
37 (27-42) 39 (27-42)

0.02

23 (82%)

49 (61%)

0.04

5 (18%)
23 (82%)

22 (28%)
58 (72%)

NS
NS

12
7
9
9

50
12
18
15

(62%)
(15%)
(23%)
(19%)

NS
NS
NS
NS

11 (14%)

NS

(43%)
(25%)
(32%)
(32%)

6 (21%)

PI: pulsatility index; NS: non-significant.

C Acta Obstet Gynecol Scand 77 (1998)

616

K. van Asselt et al.

Fig. 1. The mean pulsatility index (PI) in the two uterine arteries plotted against the degree of proteinuri.

ine artery PI showed a significant positive correlation to the degree of proteinuria at the time of
the last Doppler examination (correl. coeff.4.18;
R20.29; p0.0001), the values overlapped greatly
between different goups (Fig. 1). No relationship
was found between the uterine artery PI and the
mean maternal blood pressure at the time of examination.
The median gestational age at the last examination was 37 weeks (range 2542) and at delivery
38 weeks (range 2542 weeks). The median time
interval between examination and delivery was 3.5
days (range 025). There were 81 placentas centrally located in the uterus and 27 were mainly unilateral. In cases of unilateral placenta, the mean
uterine artery PI on the placental side was
0.850.42 (s.d.; range 0.27 to 2.43), and of the
non-placental side 1.240.65 (range 0.44 to 2.98).
Outcome of pregnancy for patients with abnormal uterine (n24) and umbilical artery (n17) PI

is given in Table II. A significantly shorter gestational age at delivery (p0.01), lower birthweight
(p0.0025) and higher birthweight deviation
(p0.0005), more SGA newborns (p0.03) and
more frequent admissions to the NICU (p0.03)
were seen in the group with abnormal PI in both
uterine and umbilical arteries when compared with
cases with abnormal PI on one side of the placenta
or with normal PI on both sides (Table II).
The perinatal outcome in relation to the occurrence of a notch in the uterine arteries is given in
Table III. When compared with cases with normal
uterine artery blood velocity, the likelihood of delivering a SGA newborn was increased eight times
in the presence of a unilateral notch and ten times
in cases with bilateral notch (Table III). In the subgroup with bilateral notches, there was a 45 times
increased likelihood of cesarean section and admission to the NICU. No relationship was found between increased placental vascular resistance and
low Apgar score or pH at delivery.
Discussion

In the present study, umbilical artery and uteroplacental Doppler velocimetry was evaluated in relation to the perinatal outcome in pregnancies
complicated by pre-eclampsia. Abnormalities on
either side of the placenta were correlated to an
unfavorable outcome of pregnancy (Tables II, III).
When comparing the groups with signs of increased vascular resistance on one side of the placenta only, with the group with abnormal vascular
resistance on both sides of the placenta, the adverse outcome of pregnancy was most frequent in
the latter group.
Proteinuria is a marker of tissue damage in preeclampsia. A significant relationship was found between the degree of proteinuria and uterine artery
PI, but no association was found between mean

Table II. Perinatal outcome in relation to the results of umbilical and uterine artery Doppler velocimetry in 108 pregnant women with pre-eclampsia. Numbers,
percentages and mean s.d. are given
Uterine artery PI:

Normal

Umbilical artery PI:

Normal

Normal

76

15

38.62.5
3352734
0.114.7
4
632173
23
12

36.52.5
2472671
16.612.1
5
44186
8
5

Number
Gestational age (weeks)
Birthweight (g)
B-weight deviat. (%)
SGA (mean - 2 s.d.)
Placental weight (g)
Cesarean section
NICU admission

Abnormal

Normal

p-value*

Abnormal

Abnormal

p-value*

8
0.005
0.0005
0.0005
0.006
0.0005
NS
NS

36.63.3
2394795
20.913
2
42692
5
5

Abnormal

p-value

9
NS
0.025
0.0005
NS
0.0005
NS
0.008

31.75.1
1351774
34.611.5
7
383166
8
8

0.0005
0.0005
0.0005
0.0001
0.0005
0.002
0.0001

PI: pulsatility index; SGA: small for gestational age i.e. birthweight below the mean - 2 s.d. of normal population; NICU: neonatal intensive care unit; NS: nonsignificant. * compared with cases with normal blood velocity on both sides of the placenta.

C Acta Obstet Gynecol Scand 77 (1998)

Doppler velocimetry in pre-eclampsia

617

Table III. Perinatal outcome according to the occurrence of uterine artery notch. Means.d. and numbers are given
Notch

Number
Gestational age (weeks)
Birthweight (g)
Birthweight deviation (%)
SGA newborns
Placenta weight (g)
Cesarean section
NICU admissions

absent

unilateral

p-value

Odds ratio
(95% confidence interval)

bilateral

p-value

Odds ratio
(95% confidence interval)

62
383
3358875
0.317
4
639187

27
373
2755784
1215
10
516136

NS
0.0025
0.0025
0.005
0.0005

8.5 (2.727)
-

19
354
2133761
2113
8
427106

0.0005
0.0005
0.0005
0.0008
0.0005

10.6 (3.235.2)
-

21
12

11
6

0.01
NS

1.3 (0.53.2)
1.2 (0.43.6)

13
10

0.009
0.007

4.2 (1.512.2)
4.6 (1.613.3)

SGA: small for gestational age i.e. birthweight below the mean - 2 s.d. of normal population; NICU: neonatal intensive care unit;
NS: non-significant. The p-values and odds ratio describe the significance of difference as compared with the subgroup with absent notches.

maternal arterial pressure and uterine artery PI.

Some of the more severe pre-eclampsia patients
were on antihypertensive medication (pindolol),
which might have decreased the blood pressure
without changing placental vascular resistance or
the degree of protein leakage in the urine and
therefore might have masked the possible relationship between uterine artery vascular resistance and
maternal blood pressure.
Biopsies from the placental bed during cesarean
section have shown that the ingrowth of cytotrophoblast into the sub-placental arteries is less advanced in cases complicated by pre-eclampsia and
IUGR than in normal pregnancies. In normal
pregnancies the sub-placental arteries can be transformed to flaccid non-contractile channels as far
as into the central part of the myometrium (19,
20). The change in the sub-placental vessels is more
pronounced under the central part of the placenta
than in the periphery. The lack of transformation
of the sub-placental vessels might cause decreased
placental perfusion, and also a release of some yet
unknown agent which increases maternal blood
pressure in order to maintain placental blood flow.
This agent has never been found, but the fact that
the disease is cured by removal of the placenta does
suggest it strongly.
The first reports on uteroplacental Doppler
velocimetry in high-risk pregnancies reported low
sensitivity for the prediction of SGA newborns (
29 to 39%) (2124). Arcuate artery blood velocity
recording was used in these studies in order to predict uteroplacental vascular resistance. As the
blood velocity waveforms were obtained blindly
from the sub-placental myometrium, a recording
might sometimes have been obtained from spiral
arteries distal to the vascular narrowing, in the dilated part of the vessel, wrongly giving the impression of normal peripheral vascular resistance
as has been described by Gudmundsson and Mar-

sal (25). Focusing on the main uterine arteries has

greatly improved the predictive value of the arterial blood velocity waveform giving sensitivities
of SGA newborns between 43 to 78% in high-risk
pregnancies (13, 15, 26, 27).
The results from the present study showed that
only 24 cases had an abnormal uterine artery PI
(22%); 32% in severe and 19% in mild pre-eclampsia groups. The corresponding percentages for the
umbilical artery velocimetry were 14%, 18% and
13%, respectively. A notch in one or both uterine
arteries was, however, more frequent, (46 cases,
43%). Although a uterine artery notch is more
common in pre-eclamptic patients than an abnormal PI, the predictive value of an early diastolic
notch seems to be inferior to an increased uterine
artery PI with regard to abnormal outcome. The
sensitivity of abnormal uterine artery PI for cesarean section delivery was 71% in the present study.
The sensitivity for a unilateral uterine artery notch
was 52% and for a bilateral notch 68%. The corresponding figures for prediction of SGA-newborns
were 50%, 30% and 42%, respectively. These results
are similar to findings by Hofstaetter et al. (15)
studying a mixed group of high-risk pregnancies,
although the sensitivities in the present study were
slightly higher.
An early diastolic notch can be a physiologic
finding till 2426 gestational weeks. In the present
study, only two women had their last examination
performed before 26 completed weeks of gestation.
Screening for uterine artery notches in mid-gestation has been reported with high sensitivity for
adverse perinatal outcome later in gestation (28,
29). Bower et al. (30) recommended a two-stage
screening of notches in the uterine arteries. First
at 1822 weeks of gestation and then at 24 weeks,
implying that abnormal blood velocity waveforms
in the uterine artery after that time were highly
predictive of adverse outcome of pregnancy. Other
C Acta Obstet Gynecol Scand 77 (1998)

618

K. van Asselt et al.

reports have been more sceptical on the use of

screening, only half of the cases that developed
pre-eclampsia or delivered a SGA infant were identified. The best results gave a 33% positive predictive value for either pre-eclampsia or SGA (31). As
only 43% of the pre-eclamptic pregnancies in the
present study had notches in the uterine arteries,
screening for pre-eclampsia before 26 weeks of gestation might therefore have unacceptably low sensitivity and a high number of false-negative cases
for a general population screening.
Previous reports have shown that abnormal
uterine artery vascular resistance can be found in
15% to 64% of cases complicated by pre-eclampsia or PIH (3236). Differences in gestational age
at the time of examination might be one factor
explaining the large variation, but differences in
blood velocity waveform parameter used for
analysis (S/D-ratio or PI), in Doppler technique
used, and populations might also be involved.
There has been a disagreement on where to
look for uterine artery abnormalities either
unilaterally, bilaterally, on the placental or on the
non-placental side of the placenta (15, 32, 36).
Kofinas et al. (36) concluded that the uterine artery PI on the placental side was the best predictor of poor perinatal outcome. In contrast Gonser et al. (37) found the uterine artery on the
non-placental side to be a better predictor of
perinatal outcome. Hofstaetter et al. (15) reported that the mean PI of both uterine arteries
PI had the best perinatal predictive value, followed by PI on placental side. The PI on the
non-placental side was the worse predictor of
outcome. The number of unilateral placentas in
the present study was 27, which is too small for
making conclusions on the choice of different
placental sites. The mean of both uterine artery
PI was therefore chosen for analysis.
The abnormal umbilical artery blood velocity
waveform was in the present study a strong predictor of adverse perinatal outcome (Table II),
which is in agreement with previous publications
(25, 32).
In conclusion, abnormal vascular resistance in
the uterine and umbilical arteries were related to
adverse outcome of pregnancies in cases complicated by pre-eclampsia. Abnormal blood velocity
waveforms on both sides of the placenta were
significantly related to adverse outcome of pregnancy characterized by premature delivery, fetal
growth restriction, more frequent cesarean sections and higher incidence of admissions to the
NICU. Utero and fetoplacental blood velocimetry might therefore be of clinical value in routine surveillance of pregnancies complicated by
pre-eclampsia.
C Acta Obstet Gynecol Scand 77 (1998)

Acknowledgments
This study was supported by the Medical Faculty, University
of Lund, the Swedish Society of Medicine, the Swedish Medical
Research Council (grant no. 5980), and University Hospital
Malmo Research Funds.

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Address for correspondence:

Saemundur Gudmundsson, M.D., Ph.D.
University of Lund
Department of Obstetrics and Gynecology
University Hospital MAS
S-205 02 Malmo
Sweden

C Acta Obstet Gynecol Scand 77 (1998)