Objective
The objective of the study was to assess the use of mean, lowest, and highest pulsatility index (PI) of the uterine arteries to screen for adverse pregnany outcome in twin pregnancies.
Study Design
This was a screening study of 423 twin pregnancies. Relationship between PI at 20-22 weeks and adverse pregnancy outcome was evaluated.
Results
Mean, lowest, and highest PI above the 95th centile were significant risk factors for preeclampsia and adverse pregnancy outcome in monochorionic and dichorionic twins. We calculated a sensitivity for preeclampsia for mean, highest, and lowest PI of 35%, 29%, and 27%, respectively.
Conclusion
Increased mean, lowest, and highest PI is associated with a higher risk of preeclampsia and adverse pregnancy outcome in twins. We observed the highest sensitivity and specificity by using highest PI. The high incidence of preeclampsia in twins makes it attractive to use the PI of the uterine artery for risk stratification in twins.
Twin pregnancies are associated with higher mortality and morbidity rates than singleton pregnancies because of higher rates of antepartum complications, preterm delivery, and uteroplacental insufficiency. In monochorionic twin pregnancies, the risk of adverse pregnancy outcome is even higher than in dichorionic twin pregnancies.
Preeclampsia is a major cause of maternal and perinatal mortality and morbidity and affects about 2% of singleton pregnancies. In twin pregnancies, the incidence of preeclampsia is 2- to 4-fold higher than in singleton pregnancies. Physiologically the trophoblast invades the spiral arteries to convert these arteries to widened channels. Normally the impedance to flow in the uterine arteries decreases between 6 and 24 weeks of gestation and remains constant thereafter.
In pregnancies complicated by preeclampsia trophoblastic invasion of the spiral arteries is impaired. Failure of trophoblastic invasion leads to a higher placental resistance. This results in altered Doppler ultrasound blood flow pattern. As a consequence the pulsatility index (PI) in the uterine arteries is increased in the first and second trimester of pregnancy. Preeclampsia can be subdivided into early and late preeclampsia. Early preeclampsia is associated with a higher risk of maternal mortality and morbidity and a higher risk of intrauterine growth restriction.
Increased uterine artery PI is associated with a higher risk of adverse pregnancy outcome even in low-risk singleton pregnancies. Measurement of uterine artery Doppler indices at 22-23 weeks of gestation in twin pregnancies could identify those at greatest risk for preeclampsia, although the sensitivity may be less than in singletons. In singleton pregnancies it has been demonstrated that not only mean PI and resistance index (RI) of the uterine arteries but also the lowest and highest PI and RI of the uterine arteries is increased in pregnancies subsequently developing preeclampsia. However, there are no studies to document the use of lowest and highest PI of the uterine arteries in twin pregnancies complicated by preeclampsia or adverse pregnancy outcome.
The aim of this study was to assess the use of mean, lowest, and highest PI of the uterine arteries to screen for preeclampsia and adverse pregnany outcome in twin pregnancies and to compare monochorionic and dichorionic twin pregnancies.
Materials and Methods
This was a screening study to evaluate the use of mean, lowest, and highest PI of the uterine arteries to assess the risk for preeclampsia and adverse pregnancy outcome because of uteroplacental insufficiency in twin pregnancies conducted at the Department of Obstetrics and Gynecology of the Medical University of Vienna, a tertiary care center serving high-risk pregnancies. The study was approved by the local ethics committee.
In our department, specialized for multiple pregnancies, 423 twin pregnancies received an anomaly scan at 20-22 weeks of gestation and were included in the study over a period of 3 years. Of the 423 pregnancies, we excluded 45 patients (10.6%): 12 (2.8%) did not receive a first-trimester ultrasound scan; in 9 pregnancies (2.1%), fetal demise before 24 weeks occurred; 14 (3.3%) underwent selective fetocide or reduction of multifetal pregnancies; in 6 pregnancies (1.4%), major fetal anomalies or chromosomal abnormalities were detected; and in 4 cases (0.9%), uterine artery PI was not measured at 20-22 weeks. Furthermore, 13 twin pregnancies (3.1%) were excluded because of missing outcome data.
The remaining 365 study patients had a first-trimester screening at 11 0 to 13 6 weeks. At this ultrasound scan, chorionicity was determined and gestational age was confirmed by the measurement of the crown-rump length of the larger twin. Chorionicity was determined according to the presence or absence of placental tissue extended into the base of the intertwin membrane before 14 weeks of gestation. In dichorionic twin pregnancies, placental tissue was visualized via ultrasound (lambda sign), and in monochorionic twin pregnancies, placental tissue was absent (T sign). Nuchal translucency thickness measurements, assessment of the nasal bone, and tricuspid valve regurgitation were used to calculate individual risks for chromosomal abnormalities. Furthermore, patients characteristics and medical history were recorded.
At 20-22 weeks, all patients had an ultrasound examination to screen for fetal anomalies. The PI of both uterine arteries was measured by transabdominal ultrasound. The uterine arteries were identified using color-flow mapping, and pulsed wave Doppler was performed at the crossover of the uterine and external iliac arteries. Care was taken that the angle of incidence was less than 30 degrees. Three similar consecutive waveforms were obtained and the PI was measured on each side. Lowest PI was defined as the lower measurement of both sides, and highest PI was defined as the higher measurement of both sides. Uterine artery Doppler measurements did not change clinical management.
From 16 weeks of gestation onward, monochorionic twin pregnancies were routinely seen at our department in 2 weekly intervals and dichorionic twin pregnancies every 4 weeks until delivery. At each visit fetal growth and the amount of amniotic fluid were assessed. Fetal Doppler values of the umbilical artery and, if necessary, the middle cerebral artery and the ductus venosus were measured. At each visit blood pressure was recorded and a urine dipstick was performed. When the pregnancy was complicated by fetal or maternal disease, additional visits were scheduled. Demographic characteristics and data on pregnancy outcome were collected from the hospital maternity records.
The main outcome measures were diagnosis of preeclampsia, which was subdivided into early (delivery before 34 weeks of gestation) and late preeclampsia (delivery after 34 weeks of gestation), and adverse pregnancy outcome including gestational hypertension, preeclampsia, fetal growth restriction below the fifth centile, placental abruption (defined as decidual hemorrhage combined with vaginal bleeding, abdominal pain and/or nonreassuring fetal heart rate pattern), stillbirth, and preterm delivery before 32 weeks. Growth charts for twins published by Voigt et al were used.
Differences between monochorionic and dichorionic twin pregnancies regarding the PI of the uterine artery were studied. Relationship between elevated mean, lowest, and highest PI and preeclampsia as well as adverse pregnancy outcome was evaluated. The sensitivity, false-positive rate, positive predictive value, negative predictive value, and likelihood ratio with 95% confidence intervals for a cutoff mean, lowest, and highest PI above the 95th centile for preeclampsia, early preeclampsia, and adverse pregnancy outcome were calculated. Furthermore, the study cohort was evaluated for the risk of preeclampsia and adverse pregnancy outcome, including the following parameters: ethnicity, maternal age, body mass index (BMI), smoking habits, parity, method of conception, chorionicity, and elevated PI of the uterine arteries.
The guidelines of the International Society for the Study of Hypertension in Pregnancy were used for definitions of gestational hypertension and preeclampsia. Gestational hypertension is defined as diastolic blood pressure of 90 mm Hg or greater on at least 2 measurements 4 hours apart developing after 20 weeks of gestation in previously normotensive women in the absence of significant proteinuria. Preeclampsia is defined as gestational hypertension and additionally proteinuria of 300 mg or more in 24 hours or 2 readings of at least ++ on dipstick analysis of midstream or catheter urine specimens if no 24 hours of collection is available.
Statistical analyses were performed with SPSS software (version 18.0; SPSS, Chicago, IL). Parametric continuous variables are summarized as means (±SD), nonparametric continuous variables as medians (minimum and maximum), and categorical data as percentages. A Kolmogornov-Smirnov test was used to identify nonparametric variables.
Categorial variables were analyzed using χ 2 or Fisher’s exact test, continuous variables were compared using unpaired Student t test, Kruskal-Wallis, and Mann-Whitney U test with post hoc Bonferroni correction for multiple testing (critical statistical significance P < .03).
Univariate and multivariate logistic regression analyses with backward selection and likelihood ratio test were performed to identify independent risk factors for preeclampsia and adverse pregnancy outcome. The goodness of fit of logistic regression models was evaluated with the Hosmer and Lemeshow test. The detection rates of all pregnancies complicated by preeclampsia, those with early preeclampsia and those with late preeclampsia, and all pregnancies with adverse pregnancy outcome were calculated and receiver-operating characteristics (ROC) curves were constructed. The area under the curve was calculated. P < .05 was considered significant.
Results
Doppler examinations of the uterine arteries were performed in 419 consecutive twin pregnancies at 20-22 weeks of gestation. After exclusion complete outcome data were available for 365 twin pregnancies, including 266 dichorionic (72.9%) and 99 monochorionic (27.1%) twin pregnancies. The mean gestational age at anomaly scan was 20.6 (±1.1) weeks of gestation.
Seven patients (1.9%) had preexisting hypertension. One hundred thirteen twin pregnancies with adverse pregnancy outcome (30.9%) were recorded: 17 patients (4.7%) had gestational hypertension, 34 patients (9.3%) developed preeclampsia, including 6 with early preeclampsia who delivered before 34 weeks of gestation (1.6%) and 28 with late preeclampsia who delivered after 34 weeks of gestation (7.7%). In 37 twin pregnancies (10.1%), fetal growth restriction was diagnosed. Two cases of stillbirth (0.5%) and 4 cases of placental abruption (1.1%) occured. A total of 42 patients (11.5%) delivered before 32 weeks ( Figure 1 ) .
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