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R. Axt-Fliedner . A. Schwarze . I. Nelles . C. Altgassen .
M. Friedrich . W. Schmidt . K. Diedrich
The value of uterine artery Doppler ultrasound in the prediction
of severe complications in a risk population
Received: 30 April 2004 / Accepted: 2 May 2005 / Published online: 3 June 2004
# Springer-Verlag 2004
Abstract Aim: The aim of this prospective study was to
assess the role of uterine artery color Doppler waveform
analysis in the prediction of adverse pregnancy outcome
such as preeclampsia, intrauterine growth retardation,
placental abruption or a combination of outcome parameters
in risk pregnancies (n=52). Methods: Various
uterine artery Doppler ultrasound parameters (resistance
index (RI)>0.58, RI>0.7 and uni/bilateral or bilateral
notching) were tested. The mean time of delivery was 37
+1 weeks’ gestation. Six newborns (12%) were delivered
before 34 weeks of gestation. The mean birth weight was
2,910 g. Dystrophic fetuses (<10% percentile) were
registered in 7 cases (13%). In 11 of the 52 women
(21%) a cesarean section was performed because of
abnormal fetal heart recording. Results: Preeclampsia
was diagnosed in 4 cases (8%). In 4 cases (8%) an
intrauterine fetal death was diagnosed. Placental abruption
did not occur. The sensitivity of notching for the
prediction of preeclampsia and for the prediction of a
severe pregnancy complication was 75 and 69% with
relative risks of 2.7 and 2.0. The sensitivity of notching in
the uterine arteries for developing an intrauterine growth
retardation (IUGR) was 71% with a relative risk of 2.2.
The sensitivity of RI>0.58 in the uterine arteries for
developing an IUGR was 67% with a relative risk of 5.4.
The sensitivity of RI>0.58 for the prediction of preeclampsia,
of intrauterine death and for the prediction of a
severe pregnancy complication was 50, 75 and 80% with
relative risks of 2.7, 8.1 and 10.9 respectively.
Conclusion The results of this study suggest that Doppler
ultrasound of the uterine artery in the second trimester of
gestation is a useful method to predict abnormal outcomes
in risk pregnancies, with high negative predictive values.
Keywords Doppler . Uterine artery . Risk population .
Screening test
Introduction
Preeclampsia and intrauterine growth retardation are one
of most common causes of fetal and maternal morbidity
and mortality, whereas their exact etiology is unknown [2, 24]. Failure of normal trophoblastic implantation, leading
to an abnormal uteroplacental blood-flow, seems to be associated with later development of preeclampsia, fetal growth restriction and placental abruption [11, 22–24]. Doppler ultrasound in the second trimester is proposed
as a potential screening test for preeclampsia and intrauterine growth retardation (IUGR), [3–9, 13]. An abnormal
uterine artery Doppler waveform reflects increased impedance in the uterine circulation that is thought to be a
secondary effect of a failed trophoblastic invasion of the muscular spiral arteries [23, 27]. In an unselected population, the presence of a diastolic notch is reported to be a
better predictor for preeclampsia than an elevated resistance index (RI), with positive predictive values (PPVs) up
to 31% [8, 16, 17]. The diagnostic accuracy of uterine
artery Doppler as a screening method for adverse pregnancy outcome is hampered by inconsistent methods, different gestational ages during examination and various definitions of study populations [9]. Furthermore, the optimal uterine artery waveform indices to obtain the best positive predictive value for preeclampsia or IUGR
remains uncertain [1, 4, 5, 21]. Performing uterine artery Doppler studies in high-risk populations for severe pregnancy complications could increase the predictive
value for adverse pregnancy outcome. Therefore, the aim
of this prospective study was to examine the value of uterine artery Doppler in a risk population for the prediction of severe pregnancy complications.
Materials and methods
In this prospective study uterine artery Doppler ultrasound was performed on women with singleton ―risk‖ pregnancies
in between 19 and 26 completed weeks’ gestation
who attended a fetal anomaly scan. The gestational age
was calculated from the first day of the last period and was confirmed by vaginal ultrasound within the first trimester. Data from 52 women were evaluated.
Women who fulfilled the following criteria were
included to the study:
–Essential hypertension (n=8)
–History of preeclampsia (n=13)
–History of intrauterine growth retardation (n=13)
–History of intrauterine death (n=28)
–History of placental abruption (n=3)
Each woman had only one uterine artery Doppler ultrasound. Multiple pregnancies or pregnancies with recognized fetal abnormalities were excluded. Doppler ultrasound was performed with the women lying in a semirecumbent position, taking care of the absence of fetal movements and a fetal heart rate between 120 and
140 bpm. Color ultrasound scan was performed with an Elegra (Siemens) and Acuson 128 XP/10 using a 3.5 or
5 MHz transducer. The high-pass filter was set at 100 Hz. The transducer end was placed on the left and right lower quadrant of the maternal abdominal wall, visualizing the external iliac artery and identifying the uterine artery medial to it. Flow velocity waveforms were obtained form each uterine artery near to the external iliac artery, before division of the uterine artery into branches, as previously described [6]. Doppler ultrasound was performed between 19 and 2
6 completed weeks’ gestation.
The presence of a diastolic notch in the flow-profiles of
the uterine arteries was noted qualitatively as a clearly definable upturn of the flow velocity, and the resistance index was calculated from five waveforms of satisfactory quality. A RI>0.58 was defined as abnormal [11, 19] and a RI>0.7 was defined as very abnormal [10, 21].
Clinical data and pregnancy outcome information were collected via a standardized questionnaire from hospital records by an investigator who classified the pregnancy outcome blinded to the Doppler results. The points to define the pregnancy outcome were: time of delivery, mode of delivery, birth weight, presence of preeclampsia (RR≥140/90 mmHg and proteinuria ≥0.3 g/24 h in the
absence of urine tract infection), intrauterine growth retardation (<10th percentile of Thompson’s scale). Placental abruption was defined as a vaginal bleeding and
evidence of fetal compromise leading to an emergency delivery and an evidence of retro-placental clot of postdelivery examination of the placenta.
―All outcomes‖ were defined as the development of preeclampsia and/or IUGR and/or IUD and/or placental abruption of any gestational age. ―Severe outcomes‖ were
defined as the development of preeclampsia and/or IUGR combined with a delivery <34 weeks and/or IUD and/or placental abruption of any gestational age [10]. Statistical analysis was performed using SPSS Version 10 for
Windows (SPSS, Chicago, IL, USA). The sensitivity, specificity, positive predictive value, negative predictive
value (NPV) and relative risk (RR) in the prediction of preeclampsia, IUGR, prematurity, placental abruption or
IUD were calculated by cross tabulation.
Table 1 Maternal characteristics of the population and pregnancy outcome
Characteristics N=52
Mean maternal age, years, median (range) 32.8 (23–46) Primiparous n (%) 2 (4)
History of abortion n (%) 28 (53)
Mean time of delivery weeks (range) 37+1 (24–41)
Delivery before the 34th week 6 (12)
Cesarean section due to pathological CTG n (%) 11 (21)
Mean birth weight, g (range) 2,910 (400–
4,300)
Fetal growth restriction <10th percentile n (%) 7 (13) Preeclampsia n (%) 4 (8)
Intrauterine death n (%) 4 (8)
Severe outcomes n (%) 6 (12%)
All outcomes n (%) 13 (25%)
Placental abruption 0
Results
General obstetric outcome data
In the period from 1999 to 2001 52 women were included
in the study. Twenty-three pregnancies (44%) had more
than one entry criterion. Mean maternal age was 32.8
(range 23–46) years. Two women (4%) were nullipara, 50 women (96%) were multiparous. Mean time of delivery
was 37+1 weeks’ gestation. Three newborns (6%) were delivered before the 34th week of gestation.
The mean birth weight was 2,910 g. Dystrophic fetuses
below <10th percentile were registered in 7 cases (13%).
Ten (19%) of the newborns had to be transferred to the neonatal intensive care unit. In 11 of the 52 women (21%)
a cesarean section due to a pathologic CTG was
performed. Preeclampsia was diagnosed in four cases (8%). Four intrauterine deaths occurred (8%). Placental abruption was not diagnosed. The mean maternal characteristics of the population and pregnancy outcome
are summarized in Table 1.
Uterine artery Doppler outcome
Fifteen women (29%) had a normal Doppler flow of the
uterine arteries. In 31 (60%) women a uni/bilateral
RI>0.58 and 14 patients (27%) a bilateral RI>0.58 could
be seen. Seven pregnancies (13%) had uni/bilateral RI
values ≥0.7 and 3 (6%) had bilateral RI values ≥0.7.
Notching was observed in 28 pregnancies (54%) uni/
bilaterally and in 15 (29%) bilaterally. The incidence of
normal and pathological Doppler ultrasound of the uterine
arteries in the examined population is shown in Table 2.
Preeclampsia
The test characteristics for predicting the development of
preeclampsia are shown in Table 3. Any notch had the
highest sensitivity with values of 75% and relative risk
2.7, respectively, whereas the positive predictive value
(11%) of any notch was low. Both RI values >0.7 detected
preeclampsia with sensitivity, specificity, positive andnegative predictive value of 25, 96, 33 and 94%,
respectively. The relative risk for preeclampsia in case of
a bilateral RI>0.7 was 5.4. Both RI values >0.58 detected
preeclampsia with sensitivity, specificity, positive and
negative predictive value of 50, 75, 14 and 95%,
respectively. The relative risk for preeclampsia in case of
a bilateral RI>0.58 was 2.7. Bilateral notching had
sensitivity, specificity, positive and negative predictive
values of 25, 71, 7 and 92%, respectively. The relative risk
in case of bilateral notching was 2.7. The sensitivity,
specificity, positive and negative predictive values as wellas the relative risk of any notching (right, left, or both
sides) was 75, 49, 11, 96% and 2.7.
Intrauterine growth retardation
The predictive values of abnormal uterine artery Doppler
waveform for IUGR were significant in case of pathological
Doppler Ultrasound (Table 4). Women with persistent
bilateral notching of the uterine arteries had a much higher
sensitivity for IUGR (71%) when compared to women
with bilateral RI>0.7 (50%) but a lower specificity (78 vs.
98%).
Both RI values >0.7 detected IUGR with sensitivity,
specificity, positive and negative predictive value of 33,
98, 67 and 92%, respectively. The relative risk for IUGR
in case of a bilateral RI>0.7 was 8.2. Both RI values >0.58
detected IUGR with sensitivity, specificity, positive and
negative predictive value of 67, 78, 29 and 95%,
respectively. The relative risk for IUGRin case of a
bilateral RI>0.58 was 5.4. Bilateral notching had sensitivity,
specificity, positive and negative predictive values
of 71, 78, 33 and 95%, respectively. The relative risk in
case of bilateral notching was 6.3. The sensitivity,
specificity, positive and negative predictive values as
well as the relative risk of any notching (right, left, or both
sides) was 71, 50, 18, 92% and 2.2. The test characteristics
for predicting IUGR are shown in Table 4.
All outcomes
The test characteristics for predicting all outcomes are
shown in Table 5. Women with both RI>0.7 had the
highest positive predictive value of 67% and relative risk
of 3.3 for an abnormal pregnancy outcome. Persistent
bilateral notching had sensitivity, specificity positive and
negative predictive values of 54, 80, 47, 84% and the
relative risk was 3.0. Women with both RI values >0.58
had the highest relative risk of 3.8 for all outcomes with
sensitivity, specificity, positive and negative predictive
values of 58, 83, 50 and 87%, respectively.
Severe outcomes
The test characteristics for predicting severe outcomes are
shown in Table 6. The sensitivities and the relative risk of
abnormal uterine waveforms were highest in this group.
Bilateral notching had the highest sensitivity with values
of 83% and relative risk 12.7, respectively, whereas the
positive predictive value (33%) was modest. Both RI
values >0.7 detected severe outcome with modest sensitivity,
but with the highest specificity, positive and
negative predictive value of 40, 98, 67 and 94%,
respectively. The relative risk for severe outcome in case
of a bilateral RI>0.7 was 10.9. Both RI values >0.58detected severe outcome with sensitivity, specificity,
positive and negative predictive value of 80, 79, 29 and
97%, respectively. The relative risk for severe outcome in
case of a bilateral RI>0.58 was 10.9. Bilateral notching
had sensitivity, specificity, positive and negative predictive
values of 83, 79, 33 and 97%, respectively. The relative
risk in case of bilateral notching for severe outcomes was
12.7.
Intrauterine death
The test characteristics for predicting intrauterine death (IUD) are shown in Table 7. Bilateral notching had the highest sensitivity with values of 75% and relative risk of 7.6, respectively, whereas the positive predictive value (20%) was modest. The highest relative risk for IUD was detected in case of bilateral RI>0.58 with 10.9. Both RI values >0.58 detected IUD with sensitivity, specificity, positive and negative predictive value of 75, 77, 21 and 97%, respectively. Both RI values >0.7 predicted IUD only with a sensitivity of 25%, whereas specificity, positive and negative predictive value were 96, 33, 94% and a relative risk for IUD was 5.4.
Discussion
In this prospective study we examined the predictive value for severe pregnancy complications of uterine artery Doppler in the second trimester in a risk population. As
a risk population we defined pregnancies by following criteria: essential hypertension, recurrent preeclampsia in previous pregnancies, history of intrauterine growth retardation, history of intrauterine death and/or history of placental abruption in previous pregnancies.
Uterine artery Doppler analysis was of limited value in the prediction of preeclampsia with predictive values of 33% in case of bilateral RI>0.7. The results were comparable to those obtained in low-risk populations [15, 25]. Others found higher predictive values in highrisk population compared to low risk women which might
be in part explained by smaller numbers in our study [7, 12, 26, 28]. However, the positive and negative predictive values for preeclampsia were better than the clinical risk evaluation based on the prevalence of preeclampsia (8%) in the study population.
Thirteen percent of the newborn were IUGR babies and the predictive performance of uterine artery Doppler was better than in a low-risk population, with positive predictive values up to 67% in the presence of bilateral RI>0.7 (RR 8.2). These data are in good accordance to those of Coleman et al. [10].
In the prediction of severe pregnancy complications requiring a delivery <34 weeks of gestation (severe outcomes) bilateral RI values >0.7 identified 67% and bilateral notching identified 33% of these women with a
sensitivity of 40 and 83%, respectively. Women with
bilateral notching and with bilateral RI>0.7 showed a
relative risk of 12.7 and 10.9, respectively for developing
a severe pregnancy complication requiring delivery before
34 weeks of gestation. The negative predictive values were
high (93–97%). Bilateral notching and bilateral RI values
>0.7 identified 47 and 67% of the women who developed
a severe complication at any gestational age. These data
confirm previous data reported by Coleman et al. [10]
In this study four intrauterine deaths occurred. Three of
four women had bilateral notching with a sensitivity and a
specificity of 75% and the predictive value of 20%
performed better than risk assessment based on the
prevalence of intrauterine fetal death (8%) in this study
population.
Impaired uteroplacental blood flow as reflected byabnormal uterine artery Doppler waveforms remains the
major cause for severe pregnancy complications, e.g.,
preeclampsia and preterm IUGR. This has lead to the idea
of uterine artery Doppler as a screening test for adverse
pregnancy outcome [13, 14, 18–20]. It can be concluded
from the published data that there is still no standardized
evaluation of what is called abnormal uterine circulation
(notch or resistance index) and when to perform the test
(20–24 weeks) in which population (low-risk or high-risk),
[9]. The subjective analysis of the absence or presence of a
diastolic notch by trained operators has good interobserver
agreement and seems to be a reliable predictor
as computerized velocity waveform analysis is still
experimental and cannot yet be transduced in a routine
clinical setting and other ratios do not perform better [1,
16].
Variations in Doppler techniques, measurement parameters
and study protocols have resulted in disappointing
results in the prediction of preeclampsia and poor
pregnancy outcome in low-risk populations [9]. The
clinical value of uterine Doppler as a screening tool in
low-risk populations is defined by the high negativepredictive value of abnormal uterine artery Doppler
waveforms.
The results of this study show that uterine artery
Doppler could be a useful method in a risk population for
the prediction of severe pregnancy complications. In any
case the test performed better than risk assessment based
on the prevalence of preeclampsia and IUGR alone.
Evaluation of uterine artery Doppler at 20–24 weeks’
gestation can be easily incorporated in the fetal anomaly
scan. Patients with bilateral notching or bilateral RI values
>0.7 at 24 weeks’ gestation represent a risk group for
adverse pregnancy outcome. On the other hand, patients
with normal flow velocity waveforms in the uterine
arteries at that time of gestation constitute a low-risk group suitable for less intensive antenatal care.
Future research should focus on further improvement to
predict adverse pregnancy outcome, e.g., by a combination
of uterine artery Doppler at 20–24 weeks’ gestation and biochemical testing (e.g., α-fetoprotein, β-human chorionic gonadotropin).
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