International Journal of Gynecology and Obstetrics 131 (2015) 4953

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International Journal of Gynecology and Obstetrics

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CLINICAL ARTICLE

Third-trimester uterine artery Doppler measurement and maternal

postpartum outcome among patients with severe pre-eclampsia
Ahmed M. Maged , Noura ElNassery, Mona Fouad, Aly Abdelhaz, Walaa Al Mostafa
Department of Obstetrics and Gynecology, Kasr AlAini Hospital, Cairo University, Cairo, Egypt

a r t i c l e

i n f o

Article history:
Received 20 October 2014
Received in revised form 17 March 2015
Accepted 4 June 2015
Keywords:
Maternal complications
Severe pre-eclampsia
Uterine artery Doppler measurement

a b s t r a c t
Objective: To evaluate the association between uterine artery Doppler measurements and maternal complications among women with severe pre-eclampsia. Methods: As part of a cross-sectional study, women with a single
intrauterine pregnancy of more than 28 weeks and a diagnosis of severe pre-eclampsia were enrolled at a unit in
Cairo, Egypt, between December 2012 and September 2014. Uterine artery Doppler was evaluated and maternal
complications were recorded. Results: Among the 100 participants, 76 (76%) experienced maternal complications. There were signicant differences in resistance index (RI) and pulsatility index (PI) between women
who experienced no complications and those who had accidental hemorrhage, HELLP syndrome, and acute
pulmonary edema (P b 0.001 for all), and postpartum hemorrhage (P = 0.004 and P b 0.001, respectively).
There was no signicant difference in RI for women with postpartum ts (P = 0.360). There was a statistically
signicant difference regarding RI (P b 0.001) and PI (P = 0.005) between cases presenting with complications
and those without. There was a signicant negative correlation between PI and gestational age (r = 0.988;
P b 0.001) and between RI and gestational age (r = 0. 854; P b 0.001), but no signicant correlation between
PI or RI and age, systolic blood pressure, or diastolic blood pressure. Conclusion: Increased uterine artery
resistance in the third trimester of pregnancy could be used to predict postpartum maternal complications.
2015 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.

1. Introduction
Pre-eclampsia is a pregnancy-specic syndrome that affects
multiple organ systems [1]. Although it is more complex than simply
gestational hypertension with proteinuria, the appearance of proteinuria remains an important and objective diagnostic criterion [2]. Preeclampsia often affects young and nulliparous women, whereas older
women are at greater risk of chronic hypertension with superimposed
pre-eclampsia [3]. Furthermore, the incidence of the disorder is markedly inuenced by race and ethnic origin, and environmental, socioeconomic, and even seasonal factors [3]. Between 3% and 10% of nulliparous
women are affected; the prevalence is lower among multiparas [4].
Pre-eclampsia is associated with a high rate of maternal and perinatal morbidity and mortality. Affected women can develop eclampsia, acute pulmonary edema, cerebral vascular accidents, and renal
and/or liver failure [5]. Pre-eclampsia is a frequent indication for
admission to obstetric intensive care units (ICUs) as well as a cause
of prolonged hospitalization [6].
The physiopathology of pre-eclampsia is believed to be poor placentation [7]. Previous reports have described the disruption of endothelial
junctional proteins [8], subendothelial ultrastructural changes in
Corresponding author at: 135 King Faisal Street, Haram, Giza 12151, Egypt.
Tel.: + 20 1005227404; fax: +20 2 35873103.
E-mail address: prof.ahmedmaged@gmail.com (A.M. Maged).

resistance arteries [9], and abnormal trophoblastic invasion and generalized vessel spasms [10]. Therefore, the uterine arteries could have
high resistance. The only known cure for pre-eclampsia is placental
delivery [11], after which the affected organ systems return to their
original state following vasospastic relief. Indeed, the role of vasoconstriction in pre-eclampsia has been well established [7] and could
explain several of the complications associated with this condition [12].
Because the persistence of bilateral early diastolic notching of the
uterine artery is a result of systemic vasospasms, a greater frequency
of complications could be expected in women in whom Doppler
velocimetry has shown the maternal compartment to be affected.
The aim of the present study was to evaluate the association
between uterine artery Doppler velocimetry indices and the frequency of maternal postpartum complications among women with
severe pre-eclampsia.
2. Materials and methods
A descriptive, observational, cross-sectional study was undertaken
at Kasr Al-Ainy Hospital Emergency Unit in Cairo, Egypt, between
December 1, 2012, and September 30, 2014. Patients with a single intrauterine pregnancy of more than 28 weeks and a diagnosis of severe preeclampsia were enrolled. Women with multiple pregnancies, a history
of chronic hypertension, gestational diabetes, diabetes mellitus, or
autoimmune diseases were excluded, as were women with uterine

http://dx.doi.org/10.1016/j.ijgo.2015.03.045
0020-7292/ 2015 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.

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A.M. Maged et al. / International Journal of Gynecology and Obstetrics 131 (2015) 4953

activity, intrauterine fetal death on admission, or clinical emergencies

with maternal hemodynamic instability or an indication for immediate
termination of pregnancy. The study was approved by the local ethics
committee. Informed consent was obtained from all participants.
The diagnosis criteria for severe pre-eclampsia were proteinuria
of more than 300 mg/mL and high systolic blood pressure (SBP;
N160 mm Hg) and diastolic blood pressure (DBP; N 110 mmHg), or a
lower SBP (N 140 mmHg) and DBP (N90 mmHg) associated with other
symptoms (e.g. a persistent headache, gastrointestinal manifestations
[vomiting], or abnormal vision). The absence of hypertension before
pregnancy and before 20 weeks of pregnancy was mandatory for diagnosis [13].
Study data were retrieved from patient and attendant interviews,
patient obstetric medical records, and referral letters in cases referred
from other health facilities. The data obtained from all women included
age, gravidity, parity, date of last normal menstrual period (to estimate
gestational age), a full medical history, and details of symptoms such
as headache, visual disturbances, epigastric pain, edema, oliguria, or
convulsions (timing and number). A full physical examination was performed. Blood pressure was measured using a mercury sphygmomanometer with appropriate size cuffs using the rst (systolic) and fth
(diastolic) Korotkoff sounds. Laboratory examinations were undertaken, including complete blood count, liver function tests (aspartate transaminase, alanine transaminase, and prothrombin activity), kidney
function tests (urea and creatinine), and blood group assessment.
Urine samples were tested for proteinuria using the dipstick method.
Transabdominal obstetric ultrasound examination was performed
using a Medison X6 machine (Medison Co, Seoul, South Korea)
equipped with a 47 MHz transabdominal probe (3D4-7EK) for conrmation of fetal number, viability, presentation, estimated fetal weight,
position and grade of placenta, amount of liquor, detailed anomaly
scan, biophysical prole, and gestational age through measurements
of the biparietal diameter, head circumference, abdominal circumference, and femur length.
Uterine artery Doppler velocimetry was performed with the
Medison X6 ultrasound scanner at the crossover of the uterine and
external iliac arteries with an insonation angle of less than 30, a velocity of more than 60 cm/s, and a sample volume of 2.0 mm. Both sides
were measured three times and the mean results were recorded. The
pulsatility index (PI) was calculated using the equation PI = (peak
systolic velocityend diastolic velocity)/time averaged velocity. The
resistance index (RI) was calculated using the equation RI = (peak
systolic velocityend diastolic velocity)/peak systolic velocity.
Management modalities included nursing care, control of convulsions using intravenous MgSO4 (6 g given intravenously over
20 minutes as a loading dose, followed by an intravenous infusion at a
rate of 1 g/hour for 24 hours, with clinical assessments every 4 hours),
control of hypertension (20 mg hydralazine diluted in 10 mL saline
given every 15 minutes until a DBP of b 100 mm Hg was reached), and
obstetric care (termination of pregnancy either by induction of labor
or through surgical interference by cesarean delivery). Women
were continuously monitored in the eclampsia ward until they were
ambulant and stable.
Continuous data were expressed as means (with standard
deviations) or number (percentage). Categorical data were presented
in the form of number and percentage. For statistical comparisons,
participants were divided by whether they presented with symptoms
and by whether they experienced complications. Comparisons between
groups (symptoms vs no symptoms, and complications vs no complications) using the Student unpaired t-test. Comparison between categorical data was performed using the 2 test. The Pearson correlation
coefcient was used to determine signicant correlations among different parameters. A receiver operating characteristic curve was used to
determine the sensitivity and specicity of endometrial volume. The
data were considered signicant if P values were equal to or lower
than 0.05 and highly signicant if P values were lower than 0.01. All

statistical calculations were performed using SPSS version 15 (SPSS

Inc, Chicago, IL, USA) for Microsoft Windows.

3. Results
A total of 100 women diagnosed with severe pre-eclampsia were
included in the present study. Among the 100 participants, 71 (71%)
presented with symptoms. The most common presenting symptoms
were headache, eclamptic ts, and epigastric pain (Table 1). Overall,
76 (76%) women experienced complications, but no maternal deaths
were recorded. The most common maternal complication was postpartum ts (Table 1). The most common fetal/neonatal complications were
neonatal ICU admission and stillbirth (Table 1).
There was a statistically signicant difference in the RI between
women without symptoms and women with ts, blurring of vision, or
coma (P b 0.001 for all), but there were no statistically signicant
differences in those with headaches (P = 0.630) or epigastric pain
(P = 0.511) (Table 2). Signicant differences in PI were observed
between women without symptoms and women with ts, blurring of
vision, or coma (P b 0.001 for all), as well as those with headaches
(P = 0.003); there was no signicant difference in those presenting
with epigastric pain (P = 0.246) (Table 2).

Table 1
Characteristics and outcomes.
Characteristic/outcome
Age, y
b20
2035
N35
Gestational age, wk
2836
N36
Presenting symptoms
Headache
Fits
Epigastric pain
Blurring of vision
Coma
Laboratory ndings
Low plateletsb
Decreased prothrombin timec
Elevated alanine transaminased
Elevated aspartate transaminasee
Elevated ureaf
Elevated creatinineg
Maternal complications
Postpartum ts
Accidental hemorrhage
Postpartum hemorrhage
HELLP syndromeh
Acute pulmonary edema
Renal failure
None
Fetal/neonatal complications
NICU admission
Stillbirth
Neonatal death
None
Body mass indexi
Proteinuria, mg/dL

Participants (n = 100)a
36 (36)
46 (46)
18 (18)
24 (24)
76 (76)
40 (40)
40 (40)
36 (36)
18 (18)
4 (4)
12 (12)
8 (8)
24 (24)
30 (30)
30 (30)
16 (16)
24 (24)
12 (12)
12 (12)
8 (8)
8 (8)
2 (2)
24 (24)
46 (46)
26 (26)
14 (14)
14 (14)
27.2 3.5
3.4 0.9

Abbreviation: NICU, neonatal intensive care unit.

a
Values are given as number (percentage) or mean SD.
b
b150 103/mL.
c
b11.4 s.
d
N30 U/L.
e
N30 U/L.
f
N6.43 mmol/L.
g
N106.08 mol/L.
h
Hemolysis, elevated liver enzymes, and low platelet count.
i
Calculated as weight in kilograms divided by the square of height in meters.

A.M. Maged et al. / International Journal of Gynecology and Obstetrics 131 (2015) 4953

51

Table 2
Correlation between resistance and pulsatility indices and maternal symptoms and complications.
RI

Presenting symptoms (n = 71)a

Fits
Blurring of vision
Headache
Epigastric pain
Coma
Maternal complications (n = 76)b
Accidental hemorrhage
Postpartum hemorrhage
Postpartum ts
HELLP syndromec
Acute pulmonary edema

PI

Mean SD

P value

Mean SD

P value

0.677 0.101
0.763 0.095
0.621 0.046
0.601 0.005
0.874 0.006

4.735
8.012
0.485
0.661
4.853

b0.001
b0.001
0.630
0.511
b0.001

2.015 0.434
2.401 0.364
1.741 0.23
1.567 0.137
2.996 0.165

8.48
7.58
3.136
1.174
4.201

b0.001
b0.001
0.003
0.246
b0.001

0.813 0.056
0.713 0.073
0.635 0.056
0.885 0.066
0.893 0.056

9.057
3.004
0.924
8.253
9.678

b0.001
0.004
0.360
b0.001
b0.001

2.540 0.377
2.188 0.094
1.872 0.206
2.654 0.477
2.705 0.377

6.163
3.530
3.054
4.397
5.263

b0.001
b0.001
0.004
b0.001
b0.001

Abbreviations: RI, resistance index; PI, pulsatility index.

a
Statistical comparisons with 29 women presenting with no symptoms (mean RI = 0.51 0.07; mean PI = 1.39 0.21).
b
Statistical comparisons with 24 women without complications (mean RI = 0.52 0.06; mean PI = 1.2 0.42).
c
Hemolysis, elevated liver enzymes, and low platelet count.

There was a statistically signicant difference in RI between women

without complications and those who experienced accidental hemorrhage, HELLP syndrome (hemolysis, elevated liver enzymes, and low
platelet count), and acute pulmonary edema (P b 0.001 for all), and
postpartum hemorrhage (P = 0.004); there was no statistically signicant difference in women with postpartum ts (P = 0.360) (Table 2).
Signicant differences in PI were observed between women without
complications and those who experienced accidental hemorrhage, postpartum hemorrhage, HELLP syndrome, and acute pulmonary edema
(P b 0.001 for all), and postpartum ts (P = 0.004) (Table 2).
There were no statistically signicant differences in RI and PI
between women with normal and decreased platelet levels, normal
and increased prothrombin times, normal and elevated urea, and normal and elevated creatinine (Table 3). Signicant differences in PI and
RI were observed between women with normal and elevated aspartate
transaminase (P b 0.001), as well as in PI between women with normal
and elevated alanine transaminase (P = 0.007) (Table 3). However, the
difference was not signicant for RI between women with normal
and elevated alanine transaminase (Table 3). Finally, there was a statistically signicant difference regarding changes in RI (P b 0.001) and PI
(P = 0.005) between cases with and without complications (Table 3).
There was a signicant negative correlation between RI and
gestational age (r = 0854; P b 0.001) (Fig. 1). There was also a significant negative correlation between PI and gestational age (r = 0.988;
P b 0.001) (Fig. 2). However, no signicant correlations were recorded
between PI or RI and age, SBP, or DBP (Table 4). Finally, there was
a signicant positive correlation between RI and PI (r = 0.854;
P b 0.001) (Fig. 3).

4. Discussion
The present study has indicated that postpartum maternal complications such as accidental hemorrhage, postpartum hemorrhage, HELLP
syndrome, and acute pulmonary edema can be predicted through
increased uterine artery resistance in the third trimester among
women with pre-eclampsia.
Pre-eclampsia is a major cause of maternal morbidity and mortality
worldwide. Among the women included in the present study, 76%
experienced maternal complications, with postpartum ts being the
most common followed by accidental hemorrhage, postpartum hemorrhage, HELLP syndrome, acute pulmonary edema, and renal failure. By
contrast, Akinola et al. [14] found that maternal complications occurred
in 26.5% of cases, acute renal failure in 14.7%, aspiration pneumonitis
in 9.6%, and cerebrovascular accident in 2.2%. These differences can be
attributed to the use of different diagnosis criteria for severe pre-

eclampsia and the fact that most patients included in the present
study came from rural areas without any prenatal follow-up.
In the present study, maternal mortality was 0%. In 1994, Douglas
and Redman [15] analyzed every case of pre-eclampsia in the UK to
assess the overall morbidity and mortality. The authors found 383
conrmed cases of pre-eclampsia with a 1.8% mortality rate [15]. By
Table 3
Comparison between normal and abnormal laboratory investigations and complications
with resistance and pulsatility indices.

Platelets
Normal
Decreaseda
t
P value
Prothrombin time
Normal
Increasedb
t
P value
Alanine transaminase
Normal
Elevatedc
t
P value
Aspartate transaminase
Normal
Elevatedd
t
P value
Urea
Normal
Elevatede
t
P value
Creatinine
Normal
Elevatedf
t
P value
Complications
No
Yes
t
P value
a
b
c
d
e
f

b150 103/mL.
N14.4 s.
N30 U/L.
N30 U/L.
N6.43 mmol/L.
N106.08 mol/L.

Resistance index

Pulsatility index

0.615 0.099
0.594 0.005
0.456
0.651

1.450 0.647
1.248 0.316
0.684
0.497

0.613 0.098
0.604 0.014
0.192
0.849

1.428 0.633
1.449 0.574
0.062
0.951

0.606 0.103
0.633 0.633
0.855
0.397

1.299 0.652
1.843 0.230
2.813
0.007

0.575 0.056
0.702 0.105
5.585
b0.001

1.123 0.402
2.146 0.426
8.104
b0.001

0.615 0.109
0.608 0.042
0.237
0.814

1.440 0.696
1.405 0.424
0.184
0.854

0.615 0.102
0.600 0.011
0.411
0.683

1.426 0.656
1.449 0.445
0.094
0.926

0.52 0.061
0.794 0.014
26.117
b0.001

1.20 0.421
1.53 0.284
2.920
0.005

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A.M. Maged et al. / International Journal of Gynecology and Obstetrics 131 (2015) 4953

r=0.846; P<0.001

Table 4
Correlations between resistance and pulsatility indices and age, systolic blood pressure,
diastolic blood pressure, and gestational age.

42

Gestational age, wk

40

Variable

38
Age
Systolic blood pressure
Diastolic blood pressure
Gestational age

36
34

Pulsatility index

P value

P value

0.207
0.155
0.095
0.846

0.149
0.283
0.510
b0.001

0.116
0.168
0.087
0.988

0.422
0.242
0.550
b0.001

32
30
28
0.3

0.4

0.5

0.6

0.7

0.8

0.9

Resistance index
Fig. 1. Correlation between resistance index and gestational age.

contrast, the maternal mortality rate reported by Akinola et al. [14] was
6.7% among patients with severe pre-eclampsia. The lower mortality
rate observed in the present study can be attributed to the availability
of high quality ICU care and physician experience in dealing with
these cases.
Schwarze et al. [16] measured various uterine artery parameters
using Doppler velocimetry in 346 pregnant women, of whom 17
(4.9%) were diagnosed with pre-eclampsia, 7 (2.0%) had maternal complications, 5 (1.4%) had a placental abruption, and 2 (0.6%) had intrauterine fetal deaths. Further, the presence of uterine artery notching
had a sensitivity of 88% in the prediction of pre-eclampsia and 62% in
the prediction of pregnancy complications with relative risks of 9.7
and 2.2, respectively [16]. These results are in agreement with those reported by de Melo et al. [17] in a study including 154 women in a teaching hospital in Recife, Brazil, in which mean uterine artery Doppler
measurements of PI (1.37) and RI (0.60) were considered high and
were predictive of prolonged hospital stay and continuation of antihypertensive drugs after discharge. Additionally, Li et al. [18] found that,
among 570 women with pre-eclampsia, 145 (25.4%) had uterine artery
notching, 88 (15.4%) had bilateral notching, and 207 (36.3%) had uterine artery notching, high PI, or both. Among 108 women with severe
pre-eclampsia, 38 (35.2%) presented with uterine artery notching [18].
Women with severe pre-eclampsia had higher vascular resistance
in uteroplacental vessels than did those diagnosed with mild preeclampsia and a higher uteroplacental vessel resistance was detected
in premature than in term pregnancies (70.9% vs. 28.4%) [18]. Finally,
the authors reported that increases in uterine artery resistance are

related to adverse pregnancy outcomes, although this nding was

present in only one-third of women with pre-eclampsia in the late
third trimester [18].
Shwarzman et al. [19] performed a prospective study to assess the
correlation between abnormal uterine artery resistance in the third
trimester of pregnancy and pregnancy outcomes, and observed a higher
rate of cesarean and preterm deliveries, small-for-gestational-age neonates, and lower Apgar scores in neonates born to women with bilateral
pathologic uterine artery Doppler waveforms than in those with normal
or pathologic unilateral waveforms. Therefore, they concluded that
abnormalities in uterine artery Doppler velocimetry detected in the
late trimester are associated with adverse perinatal outcomes in both
the presence and absence of pregnancy complications [19].
The association between uterine artery resistance in the third
trimester of pregnancy and postnatal complications has previously
been shown to arise from an extrapolation of the physiopathology of
the disease. In some studies in which the clinical expressions of preeclampsia are discussed [12], an increase in the volume of urine during
diuresis is proposed as an indicator of clinical improvement through the
resolution of vasospasms and improvement in renal perfusion. In
others, the characteristic symptoms of HELLP syndrome have been
shown to be a result of systemic vasoconstriction and the consequent
hypoperfusion to which the liver is submitted [12]. With respect to
the theory that all pre-eclampsia complications could be secondary to
hypoperfusion involving multiple organs [12], it could be inferred that
patients with a high uterine artery resistance have a more widespread
vasospastic process and would present with more evident vasoconstriction consequences.
The main limitation of the present study was the lack of patient
follow-up until the end of the puerperium. Further, it is important to emphasize that all women included in this study received a MgSO4 intravenous regimen, which could have greatly contributed toward a generally
favorable resolution in all cases. Studies such as the Magpie Trial [20]
have previously established a signicant reduction in the frequency of
complications in patients who receive MgSO4 in the peripartum period.

r=0.854; P<0.001

r=0.988; P<0.001
42

3.5

40

3.0

38

2.5

Pulsatility index

Gestational age, wk

Resistance index

36
34
32
30
28
0.0

2.0
1.5
1.0
.5

0.5

1.0

1.5

2.0

2.5

3.0

Pulsatility index
Fig. 2. Correlation between pulsatility index and gestational age.

3.5

0.0
0.3

0.4

0.5

0.6

0.7

0.8

Resistance index
Fig. 3. Correlation between pulsatility index and resistance index.

0.9

A.M. Maged et al. / International Journal of Gynecology and Obstetrics 131 (2015) 4953

The ndings of the present study indicate that third trimester

increases in uterine artery resistance can predict postpartum maternal
complications. Therefore, women presenting with increased uterine
artery resistance should be considered at high risk of complications
and should be closely monitored with swift termination of pregnancy
once fetal lung maturity is conrmed.

[9]

[10]

[11]

Conict of interest
[12]

The authors have no conicts of interest.

[13]

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