Journal of Obstetrics and Gynaecology

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Antepartum and postpartum uterine artery

impedance in women with pre-eclampsia: a case
control study

Ahmed M. Maged, Amira Y. Shoab & Amira S. Dieb

To cite this article: Ahmed M. Maged, Amira Y. Shoab & Amira S. Dieb (2019): Antepartum and
postpartum uterine artery impedance in women with pre-eclampsia: a case control study, Journal of
Obstetrics and Gynaecology, DOI: 10.1080/01443615.2018.1563054

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JOURNAL OF OBSTETRICS AND GYNAECOLOGY
https://doi.org/10.1080/01443615.2018.1563054

ORIGINAL ARTICLE

Antepartum and postpartum uterine artery impedance in women with pre-

eclampsia: a case control study
Ahmed M. Maged, Amira Y. Shoab and Amira S. Dieb
Department of Obstetrics and Gynecology, KasrAlAini Hospital Cairo University, Cairo, Egypt

ABSTRACT KEYWORDS
This is a cohort study which included 100 cases with pre-eclampsia (PE) and 100 controls, done to Pre-eclampsia; postpartum
compare the antepartum and postpartum uterine artery (UtA) Doppler velocimetry between them. UtA period; uterine artery;
PI and RI were measured before and within 48–72 h after delivery. There was a highly significant differ- Doppler ultrasound
ence between the cases and controls, regarding the UtA RI (0.70 ± 0.10 and 0.72 ± 0.10, versus
0.59 ± 0.12 and 0.60 ± 0.11) and PI (1.41 ± 0.89 and 1.45 ± 0.90 versus 0.85 ± 0.30 and 0.90 ± 0.34) meas-
ured at the antepartum and postpartum periods, respectively. Age and gestational age were signifi-
cantly related to the postpartum and changes in the UtA PI. The gestational age was also correlated to
UtA RI changes. Both the antepartum and postpartum mean blood pressure were correlated with post-
partum UtA RI and PI and PI changes after delivery. We concluded that uterine artery Doppler indices
changes are more common in women with PE, than in normotensive women with significant correla-
tions with age and gestational age.

IMPACT STATEMENT

What is already known on this subject? After delivery, the haemodynamic changes that occurred
with pregnancy reverse. Both the heart rate and the cardiac output decreased to reach the non-
pregnant state. Impedance to flow in the uterine artery rises as the nutritional needs are
decreased abruptly.

What do the results of this study add? Both the antepartum and postpartum measurement of
uterine artery Doppler indices is significantly higher in women with PE when compared to control
women. The persistent uterine artery impedance is a result of inadequate trophoblastic invasion
within the basal part of the decidua basalis and myometrium or persistently increased maternal
vascular tone.

What are the implications of these findings for clinical practice and/or further research? The
uterine artery Doppler parameters return to the non-pregnant values in normal pregnancies.
Knowing such information may help in understanding the haemodynamics of the uterine vascula-
ture during puerperium in hypertensive patients.

Introduction
uterine arteries could have high resistance (Maged
Pre-eclampsia (PE) is a unique condition which is linked to et al. 2015).
pregnancy and is characterised by a poor organ perfusion In PE, an abnormal trophoblast invasion results in an ele-
(Cunningham et al. 2014). It is totally reversible after a preg- vated pulsatility index (PI) and a proto-diastolic notch in the
nancy termination and its pathology and prognosis confirm uterine artery (Prefumo et al. 2004) with a generalised endo-
that it is a separate disease and not just unmasking of a pre- thelial trauma, an improper placental ischaemia and a result-
existing hypertension (Markham and Funai 2014) ant foetal hypoxia (Naicker et al. 2003).
PE is a two-stage pathology. It starts with the improper PE may be early onset if developed before 34 weeks of
remodelling of the endovascular trophoblasts, which subse- gestational age or late onset if developed later (Brown
quently lead to the clinical presentation of the disease et al. 2001). The early onset type is associated with a
(Maged et al. 2016). higher maternal and perinatal morbidity and mortality
The physiopathology of PE involves a poor placentation (von Dadelszen et al. 2003). The second trimesteric uter-
(Roberts and Cooper 2001), endothelial cell dysfunction and ine artery Doppler can be used not only to predict PE but
inflammation (Maged et al. 2017), subendothelial resistance also to predict non-proteinuric pregnancy induced hyper-
arteries (Suzuki et al. 2003), faulty trophoblastic invasion tension and an intrauterine growth restriction (Irion
and a generalised vasospasm (Lin et al. 1995). Therefore, the et al. 1998).

CONTACT Ahmed M. Mohamed [email protected] Department of Obstetrics and Gynecology, KasrAlAini Hospital Cairo University, 481 King
Faisal Street, Haram Giza 12111, Egypt
ß 2019 Informa UK Limited, trading as Taylor & Francis Group
2 A. M. MAGED ET AL.

Currently, the only definitive treatment for pre-eclampsia The exclusion criteria were the following: foetal chromosomal
is delivery. Treatments such as antihypertensive medication or structural abnormalities, blood loss during a delivery of
and magnesium sulphate administration for severe cases more than 500 mL, women who required blood transfusion
reduce the risk of serious complications, but the underlying or other surgical procedures during or following a vaginal
inflammatory and endothelial dysfunction processes continue delivery as a pelvic arterial embolisation and those women
to progress. For mild cases, at <37 weeks of gestation, proper with haemostasis disorders. Women with medical diseases as
antenatal care in weekly visits include the daily kick count, Diabetes, immune diseases and renal impairment, those on
reporting pre-eclampsia symptoms as headaches and visual anticoagulants or aspirin treatment during their pregnancy
symptoms to the physician by the woman, a blood pressure and those who used any forms of prostaglandins during
measurement and urine protein. A weekly laboratory evalu- labour were excluded from our study.
ation of platelets, AST, ALT, and serum creatinine (additional Our study included 200 women who were included in one
tests may be ordered as prothrombin time and concentra- of the two groups. Group I (cases) included 100 women with
tion), weekly NST, weekly amniotic fluid volume assessment, PE (60 of them were in its mild form and 40 in the severe
and an ultrasound foetal growth assessment every 2–3 weeks. form). Group II (controls) included 100 women with normo-
If pre-eclampsia with severe features, IUGR, or oligohydram- tensive pregnancy. Mild PE was defined as a new-onset blood
nios develop, admit the patient for inpatient care pressure elevation140/90 mmHg, accompanied by protein-
(Snydal 2014). uria in pregnancy (National High Blood Pressure Education
Vaginal delivery is tried in most cases, but caesarean sec- Program 2000).
tion rates increase with decreased gestational age. A regional Severe PE is diagnosed when the blood pressure is 160/
anaesthesia is preferred when needed (Cunningham 110, proteinuria >300 mg/mL, a symptomatic disease with a
et al. 2014). persistent headache, when there are gastrointestinal symp-
The task force recommends that women with pre-eclamp- toms or visual disturbances or the development of complica-
sia should have a postpartum monitoring of their blood pres- tions, such as HELLP syndrome (National High Blood Pressure
sures for 72 h in the hospital or in an outpatient clinic and Education Program 2000).
be reassessed in an office 7–10 d after delivery to detect a All of the participants were subjected to complete an
evaluation through history, examination and specific investi-
delayed postpartum pre-eclampsia and eclampsia
gations. Their blood pressure was measured twice at a rest-
(Snydal 2014).
ing position with 15 min apart using a mercury
After delivery, the haemodynamic changes that occurred
sphygmomanometer with the proper sized cuffs. We used
with pregnancy reverse. Both the heart rate and the cardiac
the first and fifth Korotkoff sounds to identify the systolic
output decrease to reach the non-pregnant state. The imped-
and diastolic blood pressure, respectively (Maged et al. 2015).
ance to flow in the uterine artery rises as the nutritional
During pregnancy, a trans-abdominal probe of a Sonoace
needs are decreased abruptly. That increase starts in the early
R3 (Samsung, Seoul, South Korea) was placed on the lower
postpartum period and continues until reaching the pre-
quadrant of the abdomen, angled medially, and colour
pregnancy state (Van Schoubroeck et al. 2004; Mulic-Lutvica
Doppler imaging was used to identify the UtA at the appar-
et al. 2007). Also, the protodiastolic notch appears again, pro-
ent crossover with the external iliac artery. Measurements
gressively (Mulic-Lutvica et al. 2007).
were taken approximately 1 cm distal to the crossover point.
The postpartum uterine artery impedance in pre-eclamptic
In all cases, once the angle was less than 30 , the pulsed
and chronic hypertensive patients was reported in many
Doppler gate was placed over the whole width of the vessel.
studies (Lee et al. 2016). No differences in uterine artery PI
Angle correction was then applied and the signal updated
between patients who had severe pre-eclampsia, as com-
until three consecutive waveforms had been obtained. Three
pared to normotensive controls. Early diastolic notch was sig- measurements were taken by the same examiner (AY) and
nificantly higher in patients following a severe pre-eclampsia. the mean of PI of bilateral UtA were taken.
The mean value of UtA PI in hypertensive women was higher We used the vaginal probe of a Sonoace R3 (Samsung,
than that in normotensive women even in the late postpar- Seoul, South Korea) for postpartum examinations of the uter-
tum period (Lee et al. 2016). ine arteries. The measurement was done at 24–72 h after
The aim of our study is to evaluate the uterine artery delivery. The participants were asked to empty their bladders
impedance before and after delivery in both healthy women and placed in the dorso-lithotomy position. The uterine
and those with PE. artery was identified at the level of the internal cervical os
with colour Doppler, and then a pulsed Doppler was used to
Materials and methods obtain the mean value of three consecutive data of the UtA
PI and PSV (Peak Systolic velocity). The same process was
A cohort study including 200 women was conducted at the repeated for the contralateral uterine artery. Three measure-
obstetric ward in KasrAlainy Hospital, Cairo University, ments were taken by the same examiner (AY) and the mean
between December 2016 and November 2017. All of the par- value of both uterine arteries was used for data analysis as a
ticipants signed an informed consent after the approval of primary outcome measure. The presence or absence of early
the KasrAlainy Ethical Committee. diastolic notches was also documented. All of the measure-
The inclusion criteria was the existence of a singleton ments were performed by a single sonographer to avoid
pregnancy, at a gestational age between 37 and 40 weeks. inter-observer variations. The sonographer scanned the same
 JOURNAL OF OBSTETRICS AND GYNAECOLOGY 3

patient again for the same antepartum and postpartum differences or more in means of postpartum uterine artery PI
measures to assess the intraobserver reliability of these meas- between hypertensive and normal deliveries. A sample size
urements. To reduce the likelihood of intraobserver bias, a calculation was done using Minitab software statistical pack-
period of at least 10 min was allowed to elapse before the age, Version 18.1 (Minitab Inc., State College, PA, 2017).
sonographer repeated the measurements.
The primary outcome parameter of our study was the
postpartum uterine artery PI. The secondary parameters
Results
included antepartum UtA PI and its change from the antepar- The flow chart of the study is shown in Figure 1. The partici-
tum to the postpartum period. pants’ characteristics showed no significant difference
The data were collected on a Microsoft Excel Sheet, 2010. between the women with PE and the control women. These
The data were statistically described in terms of the include the age, body mass index, parity and gestational age
mean ±standard deviation (±SD) or frequencies (number of (Table 1). The mean blood pressure measured during ante-
cases) and percentages when appropriate. A comparison of natal and postnatal periods and the difference between these
the numerical variables between the study groups was done two times were significantly higher in women with PE when
using the Mann–Whitney U test for independent samples. For compared to control group (Table 1).
comparing categorical data, the Chi-square (v2) test or the There was a highly significant difference between the two
exact test were performed, as appropriate. p Values of less study groups regarding the uterine artery PI measured at the
than 0.05 were considered as statistically significant using antepartum and postpartum periods being higher in women
Minitab software statistical package, Version 18.1. Minitab Inc. with PE. While the changes in PI between antepartum and
(State College, PA). postpartum measurements did not show such a difference in
To calculate the sample size, we used previously published either group (Table 1).
data (Weintraub et al. 2013) of a mean and standard devi- When comparing women with mild PE to those with a
ation of PI of the uterine artery in normal females and those severe PE, we found no difference regarding the gestational
of hypertensive deliveries (Cunningham et al. 2014) having age, the BMI, and the uterine artery PI before and after deliv-
an immediate postpartum right and left uterine artery PI ery (Table 2). There was a significant difference between the
(mean±SD) were in the patients with severe PE and controls women with a mild PE when compared to women with a
(1.69 ± 0.73 versus 1.57 ± 0.73; and 1.59 ± 0.63 versus severe PE regarding their age, parity and mean blood pres-
1.59 ± 0.55, respectively). The a-error level was fixed at 0.05 sure (measured antepartum and postpartum) and a signifi-
and the power was set at 80%. It was calculated that 99 sub- cant difference regarding their uterine artery PI changes
jects in each group should be recruited to detect 0.27 (Table 2).

230 paents (120

controls and 110
PE)

203 paents were Examined for

eligible (102 eligibility
controls and 101
PE) hypertensive)

Asked to
parcipate in the
200 paents
study
accepted (100
controls and 100PE)

Divided into two

groups

100 Controls 100 PE

Antepartum and
postpartum :
BP measurement
and Uterine
artery Doppler
Mild PE 60 Severe PE 40

Figure 1. The flow chart of the study.

4 A. M. MAGED ET AL.

Table 1. Clinical characteristics and uterine artery Doppler of the studied population.
Sample population PE group Control group
Variable (N ¼ 200) (N ¼ 100) (N ¼ 100) p Value
Age (years) 28.70 ± 5.07 29.31 ± 5.11 28.08 ± 4.97 .09
Gestational age (weeks) 37.67 ± 1.36 37.49 ± 1.63 37.84 ± 1.34 .09
Nullipara a 79 (39.5%) 42 (42%) 37 (37%) .47
BMI (kg/m2) 27.6 ± 6.39 28.27 ± 4.36 28.94 ± 7.92 .77
Infant birth weight (in kg.) 3.01 ± 0.59 2.90 ± 0.64 3.11 ± 0.52 .011a
Mean BP (mmHg)
Antepartum 103.06 ± 17.94 118.93 ± 10.02 87.25 ± 6.51 <.001a
Postpartum 95.59 ± 13.07 104.87 ± 11.50 86.32 ± 6.13 <.001a
Changes 7.47 ± 8.59 –14.07 ± 6.81 –0.93 ± 3.95 <.001a
Uterine artery PI
Antepartum 1.13 ± 0.72 1.41 ± 0.89 0.85 ± 0.30 <.001a
Postpartum 1.18 ± 0.73 1.45 ± 0.90 0.90 ± 0.34 <.001a
Changes 0.05 ± 0.24 0.04 ± 0.30 0.05 ± 0.18 .634
Data are presented as mean ± SD.
a
Data are presented as number (percentage).
PE: pre-eclampsia; BMI: body mass index; BP: blood pressure; PI: Pulsatility Index, significant when p < .05.

Table 2. Clinical characteristics of the severe and mild types of PE. needed in the first weeks after delivery, how quickly and
Severe PE Mild PE accurately these dynamic changes in blood return to those in
Variable (N ¼ 40) (N ¼ 60) p Value the non-pregnant state can explain our results (Guedes-
Age (years) 28.25 ± 4.17 30.017 ± 5.568 .034 Martins et al. 2015).
Gestational age (weeks) 37.53 ± 1.47 37.117 ± 1.354 .36
Nulliparaa 12 (30%) 30 (50%) .045a
In our study, we included pregnancies that terminated
BMI (kg/m2) 28.26 ± 4.31 27.88 ± 4.38 .41 vaginally, those delivered by CS were excluded as it was
Neonatal birth weight (in kg.) 2.69 ± 0.62 3.04 ± 0.62 .008a demonstrated that spinal anaesthesia decreases the uterine
Mean BP (mmHg)
Antepartum 127.42 ± 9.70 113.17 ± 4.67 <.001a artery PI in hypertensive women (Guedes-Martins et al. 2014).
Postpartum 115.83 ± 7.08 97.56 ± 7.26 <.001a Age specific trends in the prevalence of a mild pre-
Changes –11.75 ± 5.20 –15.61 ± 7.13 .004a eclampsia showed that its rate decreased among women
Uterine artery PI
Antepartum 1.48 ± 0.46 1.37 ± 1.09 .313 aged <30 years, whereas the rate increased among the older
Postpartum 1.65 ± 0.48 1.32 ± 1.08 .440 women, e.g. among 30–34-year-old women (Ananth et al.
Changes 0.16 ± 0.18 –0.05 ± 0.32 <.001a 2013). Age correlated significantly with post-partum UtA PI
Data are presented as mean ± SD. and its changes between the ante- and post-partum periods
a
Data are presented as number (percentage).
PE: pre-eclampsia; BMI: body mass index; BP: blood pressure; PI: Pulsatility (Table 3). This correlation has been studied in normal preg-
Index, significant when p < .05. nancy and was found statistically non-significant (Guedes-
Martins et al. 2015). No studies are available on hypertensive
pregnancy, regarding these relations.
The analysis was performed in women with late pre- Significant differences were found in the infant birth
eclampisa and the findings may be different in early onset weight between the pre-eclamptic and control groups, as
pre-eclampsia. Table 3 shows the correlation between differ- well as between the severe and mild subgroups (Tables 1
ent characteristics and postpartum uterine artery Doppler and 2). This is explained by the significant defects in the
parameters and their changes after delivery. Age and gesta- trophoblast invasion of the decidua that lead to direct effects
tional age were significantly related to the postpartum and on the foetus, such as intrauterine growth restriction
changes in uterine artery PI. Both the antepartum and the (Snydal 2014).
postpartum mean blood pressure were correlated with the Both the antepartum and the postpartum measurement of
postpartum UtA PI and PI changes after delivery. The ante- uterine artery Doppler indices is significantly higher in
partum uterine artery RI was significantly correlated to the women with PE when compared to control women. The per-
postpartum PI (Table 3). sistent uterine artery impedance is a result of inadequate
trophoblastic invasion within the basal part of the decidua
basalis and myometrium (Cunningham et al. 2014) or persist-
Discussion
ently increased maternal vascular tone. Also, atherosis of pla-
The process involves a spiral artery luminal obliteration due cental bed spiral arterioles can cause a decrease in placental
to phenomena such as thrombosis, endarteritis and intima perfusion (Redman and Sargent 2003).
thickening, which result in an increased local vascular resist- In the antepartum and postpartum periods, the change in
ance. Although this finding may reflect systemic circulatory uterine artery PI was not significantly different between the
changes, an immediate cause for the events is the mechan- PE group and control group. This agrees with the results of
ical pressure imposed by the contracted postpartum myome- Lee et al.’s study in antepartum and immediate postpartum
trium, as well as, possibly, local immunological phenomena periods values of the mean UtA PI in both groups of study. A
(Guedes-Martins et al. 2015). longer period of follow-up is needed, as it would take several
Although significant changes occur in the pelvic circula- weeks for uterine artery Doppler indices to return to the
tion because pregnancy blood requirements are no longer non-pregnant state, as found in studies on the uterine artery
 JOURNAL OF OBSTETRICS AND GYNAECOLOGY 5

Table 3. The p values and Pearson’s correlation between different characteristics of patients with Pre-eclampsia, postpartum uterine artery Doppler PI,
and changes.
Variable Statistical test Postpartum uterine artery PI (N ¼ 100) The change in uterine artery PI (N ¼ 100)
Age Pearson’s correlation –0.586 0.277
p Value <.001 .005
Gestational age Pearson correlation –0.083 –0.221
p Value .41 .027
BMI (kg/m2) Pearson’s correlation –0.014 –0.046
p Value .893 .651
Neonatal birth weight (in kg) Pearson’s correlation –0.038 0.03
p Value .706 .77
Antepartum mean BP Pearson’s correlation 0.203 0.278
p Value .043 .005
Postpartum mean BP Pearson’s correlation 0.320 0.260
p Value .001 .009
The change in mean BP Pearson’s correlation 0.247 0.031
p Value .013 .760
Antepartum uterine artery PI Pearson’s correlation 0.947 –0.137
p Value .947 .175
Significant when p value is <.05.

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