Evaluation of the predictive value of fetal Doppler ultrasound for neonatal outcome from the 36th week of pregnancy
Zahra Laleh Eslamian1, Elahe Zarean2, Maryam Moshfeghi1, Zahra Heidari3
1 Department of Obstetrics and Gynecology, Fetal Medicine Unit, Tehran University of Medical Sciences, Tehran, Iran
2 Department of Obstetrics and Gynecology, Fetal Medicine Unit, Isfahan University of Medical Sciences, Isfahan, Iran
3 Department of Biostatistics and Epidemiology, School of Health, Isfahan University of Medical Sciences, Isfahan, Iran
|Date of Submission||13-Feb-2017|
|Date of Decision||13-Aug-2017|
|Date of Acceptance||08-Nov-2017|
|Date of Web Publication||20-Feb-2018|
Dr. Elahe Zarean
Department of Obstetrics and Gynecology, AL-Zahra Hospital, Sofe Boulevard, Isfahan
Source of Support: None, Conflict of Interest: None
Background: Early prediction of adverse neonatal outcome would be possible by Doppler impedance indices of middle cerebral artery (MCA), umbilical artery (UmA), and descending aortal artery (AO) that result in decrease neonatal morbidity and mortality rate. The aim of the present study was a determination of optimal value for the ratio of MCA to descending aorta blood flow (MCA/AO) impedance indices and its comparison with the ratio of MCA to UmA (MCA/UmA) impedance indices and their relationship with neonatal outcome. Materials and Methods: This was a prospective cohort study on 212 pregnant women with gestational age 36 weeks or more, in three hospitals in Tehran, from April 2012 to April 2013. We investigated AO, MCA, and UmA impedance indices Doppler ultrasound every 2 weeks till delivery. The mother was monitored for adverse pregnancy outcome (hypertension [HTN], fetal growth retardation, and other maternal complications) then infant birth weight, cord blood of pH, and Neonatal Intensive Care Unit (NICU) admission during the first 24 h after delivery were assessed. Finally, we investigated relationships between Doppler indices and neonatal outcomes include neonatal body weight (NBW), cord blood of pH, and NICU admission. Results: MCA/AO resistance index (RI) and MCA/AO pulsatile index (PI) showed an area under the receiver operating characteristics curve (area under the curve) of 0.905 (95% confidence interval (CI): 0.850, 0.959) and 0.818 (95% CI: 0.679, 0.956), respectively. The cutoff values for pH (≥7.2 vs. <7.2) based on MCA/AO RI and MCA/AO PI indices were 0.951 (sensitivity, 80% and specificity, 86%) and 0.853 (sensitivity, 91% and specificity, 83%), respectively. The cutoff value for NBW (≥2500 vs. <2500 g) based on MCA/UmA PI index was 1.467 (sensitivity, 73% and specificity, 63%). The cutoff value of NICU admission of child based on MCA/AO PI index was 1.114 (sensitivity, 73% and specificity, 54%). Conclusion: In the end of third-trimester pregnancies with the assessment of MCA and AO artery Doppler ultrasonography, it is possible to prevent many cases of neonatal acidosis caused by prenatal asphyxia as well as inappropriate interventions which are applied on mother. If MCA/AO PI was <0.85, the fetus needs to be evaluated further because it is at risk for acidosis.
Keywords: Complicated pregnancy, Doppler indices, neonatal outcome uncomplicated pregnancy
|How to cite this article:|
Eslamian ZL, Zarean E, Moshfeghi M, Heidari Z. Evaluation of the predictive value of fetal Doppler ultrasound for neonatal outcome from the 36th week of pregnancy. J Res Med Sci 2018;23:13
|How to cite this URL:|
Eslamian ZL, Zarean E, Moshfeghi M, Heidari Z. Evaluation of the predictive value of fetal Doppler ultrasound for neonatal outcome from the 36th week of pregnancy. J Res Med Sci [serial online] 2018 [cited 2018 Dec 19];23:13. Available from: http://www.jmsjournal.net/text.asp?2018/23/1/13/225898
| Introduction|| |
There are studies to show effectiveness at improving perinatal outcomes with the application of fetal well-being tests result in prediction neonatal outcome. The neonatal outcome contains body weight, cord blood pH at delivery, and admission of Neonatal Intensive Care Unit (NICU) that determinate timing of delivery, places of delivery (first, secondary, or tertiary center), and necessary personnel and equipment to get ready for the delivery high-risk neonate.
In the past decades, color Doppler ultrasound has been employed for fetal surveillance.,, Doppler studies are noninvasive and help to identify the degree of placental insufficiency and also to detect worsening of the situation, thereby decision to intervene can be taken once the need arises. The results of umbilical artery (UmA) Doppler is a reflection of the placenta status, whereas the results obtained from a middle cerebral artery (MCA) and aorta artery indicate the state of fetal circulation. Doppler ultrasound is used in high-risk pregnancies, particularly the cases complicated by fetal growth retardation, preeclampsia, or other maternal medical conditions., Abnormal MCA Doppler alone showed limited predictive accuracy for compromise of fetal and neonatal well-being.,, Today, according to the evidence available, Doppler study of the umbilical arteries is the only test that has shown to improve the outcome, reducing perinatal mortality, and reducing obstetric interventions.
After the 34th week of gestational age, cerebroplacental ratio is not significantly related with the prognosis and outcome of the pregnancy., Therefore, during the 3rd trimester, the ratio of pulsatile index (PI) and resistance index (RI) of MCA to the descending aorta could be used. This is while various studies have shown that, as the gestational age increases, contrary to other vasculatures, the vascular resistance of descending aorta is kept unchanged.,,,, Hence, Doppler indices of this artery could be used for investigation of the hemodynamic status, especially after the 34th week of pregnancy.
The studies on the ratios of blood flow in the descending aorta and cerebral arteries have tried to carry out better evaluations on the unfavorable fetal conditions and oxygenation level in small-for-gestational-age fetuses. However, no guidelines are currently available on clinical and physiological determination of fetal arterial circulation, particularly around the end of pregnancy.
The aims of the current study are a diagnosis of placental dysfunction and fetal hypoxia and determination of the predictive value of Doppler ultrasound for neonatal outcome in complicated and uncomplicated pregnancies in late pregnancy with regard to the blood flow indices as long as prevent neonatal asphyxia.
| Materials and Methods|| |
This was a prospective cohort study on pregnant women in three university hospitals in Tehran, from April 2012 to April 2013. This study was approved by the Ethics Committee within Tehran University of Medical Sciences.
All of the pregnant women with gestational age 36 weeks who came to prenatal clinic for prenatal care and completed the consent form were included in the study. Multiple pregnancies and pregnancies with major fetal anomalies were excluded. For each mother, the demographic characteristics were recorded as well as the reason for referral, history of medical disorders before or during the pregnancy, and familial medical history in a datasheet. The gestational age was calculated according to the regular and reliable last menstrual period, which was found consistent with the crown-rump length reported in the first-trimester ultrasound. If a mother had a medical disorder, a complete history of the condition, a list of drugs taken, and the disease history before and during the pregnancy were recorded.
An ultrasound follow-up with biometric measurement and MCA, UmA and descending (abdominal) aorta Doppler studies was scheduled every 2 weeks till delivery by Siemens ultrasound machine, Antares. During the evaluation, RI, PI, and systolic to diastolic standard deviation (SD) ratio of each artery were measured. Moreover, the mothers were followed for complications such as fetal growth restriction (FGR), preeclampsia, placental abruption, and fetal distress until delivery. For all participants, the history of labor, peripartum hypoxic events, the cause of delivery or cesarean section, neonatal UmA pH, and birth weight (BW) and neonatal sex, follow-up during the first 24 h after delivery was recorded.
According to methodology of Doppler assessment of fetal arteries from “Doppler in obstetrics” in ISOUG educational series, the Doppler indices were measured using an abdominal probe while the mother lies in a semi-recumbent position with a slight lateral tilt, and according to evaluation of the UmA, MCA, and abdominal aortal artery (AO) (just below the bifurcation of renal arteries).,
After collecting the data, the pregnant women were categorized into two groups; 1 - complicated group contains “FGR, hypertensive disorder, and vasculopathy depend on overt diabetes or systemic lupus erythematosus (SLE) or renal disease” and 2 - uncomplicated group (low-risk pregnancy). Results of the Doppler ultrasound (MCA/AO RI and PI and MCA/UmA RI and PI) and neonatal body weight (NBW), cord blood of pH, and NICU admission in these two groups were analyzed. The neonate is poor outcome with pH <7.2 and NBW <2500 g and NICU admission after than birth but if pH ≥7.2 and or NBW ≥2500, she or he can be a good outcome.,
The Kolmogorov–Smirnov (K-S) test was used to evaluate the normality of the quantitative data. Quantitative and qualitative variables were presented as mean ± SD or median and interquartile range (IQR), as appropriate, and number (percent), respectively. Independent Student's t-test was used to compare quantitative variables among studied groups. Distribution of study participants in terms of categorical variables was compared between two groups using the Chi-square test. The Pearson correlation coefficient was used to examine relationships between Doppler indices and neonatal outcomes. Receiver operating characteristics (ROC) curves were used to determine the predictive value of Doppler indices for neonatal outcomes. In addition, odds ratios (ORs) obtained from logistic regression describe associations of Doppler indices with neonatal outcomes. Data analyses were performed using Statistical Package for the Social Sciences software version 21 (SPSS Inc., Chicago, IL, USA).
| Results|| |
In this study, 212 pregnant women were evaluated. Among them, 65 (30.7%) were complicated by fetal growth retardation, hypertensive disorder, and vasculopathy due to overt diabetes or SLE or renal disease. The mean age was 28.12 ± 5.11 years (27.98 ± 4.88 and 28.43 ± 5.63 years for uncomplicated and complicated groups, respectively; P > 0.05). Median gestational age at delivery was 37 weeks, 4 days (IQR: 36 weeks, 4 days to 38 weeks, 4 days), 37 weeks, 4 days (IQR: 37 weeks, 4 days to 39 weeks, 4 days), and 37 weeks, 4 days (IQR: 36 weeks, 4 days to 37 weeks, 4 days) for uncomplicated and complicated groups, respectively).
About 8% of women were underweight, 28.3% overweight, and 12.7% obese. Family history of diabetes, heart disease, and thrombophilia was reported in 9.5% of women (6.9% and 15.4% for uncomplicated and complicated groups, respectively; P = 0.053). Delivery was performed by cesarean section in 67% of women (64.8% and 71.9% for uncomplicated and complicated groups, respectively, P = 0.318). Thirty neonates (14.4%) were admitted to NICU (11 (7.5%) and 19 (30.2%) for uncomplicated and complicated groups, respectively P < 0.0001. Nearly 57.1% of women were primary gravid (55.1 and 61.5 for uncomplicated and complicated groups, respectively). Median BW was 3100 g (IQR: 2738.75–3500 g); 3250 g (IQR: 2900–3600 gr), and 2650 g (IQR: 2240–3200 g) for uncomplicated and complicated groups, respectively, P < 0.0001. There were statistically significant differences between two groups in terms of umbilical cord pH and Doppler indices (MCA/AO PI, MCA/UmA RI, and MCA/UmA PI) (P< 0.05) so that mean of mentioned indices in complicated group was lower than the other group [Table 1].
|Table 1: Demographic and obstetric characteristics of study participants|
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The correlation of analyzed results for assessing the relationship between Doppler indices with umbilical cord pH and NBW was presented in [Table 2]. Doppler indices (i.e. MCA/AO RI, MCA/AO PI, MCA/UmA RI, and MCA/UmA PI) correlated significantly with umbilical cord pH. Among them, MCA/AO PI had stronger associations with umbilical cord pH (r = 0.411 and 0.510 for total sample and complicated group, respectively, P < 0.01). MCA/UmA PI index was significantly correlated with NBW (r = 0.253 and 0.376 for total sample and complicated group, respectively, P < 0.01).
|Table 2: Pearson correlation between Doppler indices with pH and neonatal body weight|
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Mean ± SD of Doppler indices according to status of NICU admission is presented in [Table 3]. Mean of MCA PI/AO PI index for mothers of neonates admitted to NICU was significantly lower than others in total sample and complicated group (P< 0.05). Furthermore, mean of MCA/UmA PI index for mothers of neonates admitted to NICU was significantly lower than others in complicated group (P< 0.05).
|Table 3: Comparing mean of Doppler indices according to status of Neonatal Intensive Care Unit admission|
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ROC curves for pH (≥7.2 vs. <7.2) based on Doppler indices are shown in [Figure 1], [Figure 2], [Figure 3], [Figure 4]. MCA RI/AO RI showed an area under the ROC curve (area under the curve [AUC]) of 0.818 (95% CI: 0.679, 0.956), 0.966 (0.93, 1.00), and 0.729 (0.53, 0.93) for total sample, uncomplicated, and complicated groups, respectively [Table 4]. The optimal cutoff point was 0.951 (sensitivity, 80% and 100%; specificity, 86% and 88%) for both total sample and uncomplicated group and 0.827 (sensitivity, 69%; specificity, 90% and 88%) for complicated group [Table 4]. MCA/AO PI index showed an area under the ROC curve (AUC) of 0.905 (95% CI: 0.850, 0.959), 0.940 (0.893, 0.986), and 0.870 (0.774, 0.965) for total sample, uncomplicated, and complicated groups, respectively [Table 4]. The optimal cutoff point was 0.853, 0.849, and 0.880 (sensitivity, 91%, 100%, and 86%; specificity, 83%, 84%, and 80%) for total sample, uncomplicated, and complicated groups, respectively [Table 4]. By comparing the ORs of the four indices and their corresponding 95% confidence interval (CI), again MCA/AO PI demonstrates the highest discriminating power compared to other indices for pH (OR: 0.09, 95% CI [0.05–0.15]) [Table 4].
|Figure 1: Receiver–operating characteristics curve for pH and middle cerebral artery resistance index/aortal artery resistance index|
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|Figure 2: Receiver operating characteristics curve for pH and middle cerebral artery pulsatile index/aortal artery pulsatile index|
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|Figure 3: Receiver operating characteristics curve for pH and middle cerebral artery resistance index/umbilical artery resistance index|
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|Figure 4: Receiver operating characteristics curve for pH and middle cerebral artery pulsatile index/umbilical artery|
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|Table 4: Odds ratios and diagnostic criteria of receiver operating characteristics curve for Doppler indices|
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ROC curve analysis for NBW (≥2500 vs. <2500 g) is shown in [Figure 5] and [Figure 6]. MCA/UmA PI showed an AUC of 0.722 (95% CI: 0.625, 0.819) and 0.748 (0.627, 0.869) for total sample and complicated group, respectively [Table 4]. The optimal cutoff point was 1.467 and 1.471 (sensitivity, 73% and 81%; specificity, 63% and 62%) for total sample and complicated group, respectively [Table 4]. In addition, by comparing the ORs and their corresponding 95% CI, MCA/UmA PI demonstrates the highest discriminating power for NBW (OR: 3.39, 95% CI [2.57–4.56]) [Table 4].
|Figure 5: Receiver operating characteristics curve for neonatal body weight and middle cerebral artery resistance index/umbilical artery resistance index|
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|Figure 6: Receiver operating characteristics curve for neonatal body weight and middle cerebral artery pulsatile index/umbilical artery pulsatile index|
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ROC curve for NICU admission of the child based on MCA/AO PI is shown in [Figure 7]. The optimal cutoff point was 1.114 and 1.07 (sensitivity, 73% and 79%; specificity, 54% and 55%) for total sample and complicated group, respectively [Table 4].
|Figure 7: Receiver operating characteristics curve for Neonatal Intensive Care Unit admission and middle cerebral artery pulsatile index/aortal artery pulsatile index|
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| Discussion|| |
In this study with investigation of impedance indices of MCA, UmA, and aorta artery Doppler between 36 and 41 weeks of pregnancy, we understood that cerebroaortic ratio (CAR) is in relation with neonatal acidosis and admission at NICU compared with other impedance indices, especially cerebral-placenta ratio (CPR) but NBW is in more relation with that. Therefore, with the assessment of CAR at the end of third trimester and especially in high-risk pregnancies compromise fetus is predictable. After 36 weeks, MCA/AO PI < 0.85 indicates the possibility of hypoxia in the fetus, which means that the fetus should be placed under special care and should be born early if needed, also the birth should be done at the tertiary center.
Hence, with more intervention, neonatal hypoxia and acidosis are preventable.
The studies which have used Doppler indices for adverse pregnancy outcome (APO) are divided into two groups: 1 - the studies which have been done in normal pregnancy ,, such as the systematic review done by Alfirevic et al. in 2015. In this research, conclusive evidence was not seen for the use of routine UmA Doppler ultrasound in favor of mother and baby. In another research by Akolekar et al. in 2015 on 6178 pregnancies between 35 and 37 weeks, it was concluded that the CPR assessment in routine screening for APO is poor at 36-week gestation. However, in a small subgroup, if delivery was done in 2 weeks after Doppler ultrasound, the detection rate of CPR was increased. In our research, the unselected population at the end of the third trimester was the same as the study done by Akolekar. However, CAR was used in our research instead of CPR and was valuable for neonatal outcome.
2 - The studies which have been done in high-risk pregnancies, especially pregnancies with FGR and HTN., Alfirevic's research in 2013 suggested that the use of Doppler ultrasound in high-risk pregnancies decreased the risk of perinatal death and resulted in less obstetric intervention, but it did not have any effect on Apgar scores <7 at 5 min of birth. The research was done by Rozeta in 2010 on pregnancies with preeclampsia and gestation HTN. And also, the study was done by Chalubinski in 2012 on FGR pregnancy, CPR was in relation with APO. Most studies of Doppler ultrasound have been done on FGR, but according to Bakalis et al. in a research on 30,780 singleton pregnancy between 30 and 34 weeks, it was observed that APO was more related to AGA not SGA, and the cases with umbilical cord pH ≤ 7 or admission to NICU were more seen in AGA group. Therefore, if APO is the result of impaired placentation, prenatal care must be done to identify hypoxic fetus not fetal weight.
In previous studies, Doppler indices in FGR and HTN pregnancies were into account, but in the present stud, y Doppler indices were used to predict neonatal outcome in low-risk and high-risk pregnancies which are almost the same as Akolekar's research in 2015, but the main difference is that, in this study, aortal indices were used and compared with UmA indices at the end of the third trimester. A few studies were done on Aortal Doppler indices and its relation to neonatal outcome and APO such as Aranyosi et al.'s research in 2001 which investigated MCA and aortal Doppler between the 28th and 41st week of gestation. It was concluded that if AO/MCA RI was constant during this period of uncomplicated pregnancy, it reflects optimal perinatal results and if this ratio is abnormal, it has a strong association with fetal hypoxia.
This relation is also seen in our study; however, PI has more relation with fetal hypoxia compare to RI. Furthermore, Aranyosi et al. did another research on 96 uncomplicated pregnancies between the 38th and 40th weeks of gestation, and they reported the normal AO/MCA RI as 1.06 ± 0.08 and aortic-cerebral RI (ACRI) in normal pregnancies was below 1.2 but ACRI above 1.2 was not assessed. In comparison, in our research, the related cutoff was 1.05 in the entire population and also in the uncomplicated group and was 1.2 in complicated group, which was similar to that of Aranyosis's work. The novel observation in our study was a comparison of CPR with CAR in duration of 2 weeks and the strong relation of CAR with neonatal outcome. As long as UmA impedance indices from 36 weeks on have less value for APO and neonatal outcome; in this gestational age, aortal impedance indices must be used.
Finally, in normal- and high-risk pregnancies, CAR is in strong relation with cord blood pH at delivery and admission of NICU; however, NBW is in association with CPR.
| Conclusion|| |
This research showed that, with an assessment of MCA/AO PI in late pregnancy can be prevented of stillbirth due to asphyxia and so neonatal ischemic, hypoxic encephalopathy, on the other side, obstetric intervention is also prevented.
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Conflicts of interest
There are no conflicts of interest.
| References|| |
O'Neill E, Thorp J. Antepartum evaluation of the fetus and fetal well being. Clin Obstet Gynecol 2012;55:722-30.
Alfi revic Z, Stampalija T, Gyte GM. Fetal and umbilical Doppler ultrasound in high-risk pregnancies. Cochrane Database of Systematic Reviews 2013; 11: CD007529.
Scherjon SA, Smolders-DeHaas H, Kok JH, Zondervan HA. The “brain-sparing” effect: Antenatal cerebral Doppler findings in relation to neurologic outcome in very preterm infants. Am J Obstet Gynecol 1993;169:169-75.
Mandruzzato G. Obstetrical Doppler: The evidence today. J Perinat Med 2015;43:129-31.
Rekha BR, Pavanaganga A, Sai Lakshmi MP, Nagarathnamma R. Comparison of Doppler findings and neonatal outcome in fetal growth restriction. Int J Reprod Contracept Obstet Gynecol 2017;6:955-8.
Morris RK, Selman TJ, Verma M, Robson SC, Kleijnen J, Khan KS, et al.
Systematic review and meta-analysis of the test accuracy of ductus venosus Doppler to predict compromise of fetal/neonatal wellbeing in high risk pregnancies with placental insufficiency. Eur J Obstet Gynecol Reprod Biol 2010;152:3-12.
Creasy RK, Resnik R, Iams JD, Lockwood CJ, Moore TR, Greene MF. Maternal-Fetal Medicine. 7th
ed. Philadelphia: Elsevier; 2014.
Morris RK, Say R, Robson SC, Kleijnen J, Khan KS. Systematic review and meta-analysis of middle cerebral artery Doppler to predict perinatal wellbeing. Eur J Obstet Gynecol Reprod Biol 2012;165:141-55.
Khalil AA, Morales-Rosello J, Elsaddig M, Khan N, Papageorghiou A, Bhide A, et al.
The association between fetal Doppler and admission to neonatal unit at term. Am J Obstet Gynecol 2015;213:57.e1-7.
Morales-Roselló J, Khalil A, Morlando M, Bhide A, Papageorghiou A, Thilaganathan B, et al.
Poor neonatal acid-base status in term fetuses with low cerebroplacental ratio. Ultrasound Obstet Gynecol 2015;45:156-61.
Harrington K, Thompson MO, Carpenter RG, Nguyen M, Campbell S. Doppler fetal circulation in pregnancies complicated by pre-eclampsia or delivery of a small for gestational age baby: 2. Longitudinal analysis. Br J Obstet Gynaecol 1999;106:453-66.
Baschat AA. Descending arterial and venous Doppler in the diagnosis and management of early onset fetal growth restriction. Early Hum Dev 2005;81:877-87.
Aranyosi J, Bettembuk P, Zatik J, Ovári L, Török I, Gódény S, et al.
Doppler evaluation of the fetal arterial circulation: Reference values of the Resistance Index and Pulsatility Index between the 28th
weeks of gestation. Orv Hetil 2001;142:1847-50.
Nishihara R, Nakai Y, Tachibana D, Yamamasu S, Iwanaga N, Ishiko O, et al.
Effects of different sampling points on evaluation of fetal descending aortic flow. Osaka City Med J 2006;52:39-45.
Konje JC, Abrams KR, Taylor DJ. Normative values of Doppler velocimetry of five major fetal arteries as determined by color power angiography. Acta Obstet Gynecol Scand 2005;84:230-7.
Marsál K, Laurin J, Lindblad A, Lingman G. Blood flow in the fetal descending aorta. Semin Perinatol 1987;11:322-34.
Bilardo CM, Campbell S, Nicolaides KH. Mean blood velocities and flow impedance in the fetal descending thoracic aortic and common carotid artery in normal pregnancy. Early Hum Dev 1988;18:213-21.
Nicolaides K, Rizzo G, Hecher K, Ximenes R. Doppler in Obstetrics. London: The Fetal Medicine Foundation; 2002.
Schmidt KG, Di Tommaso M, Silverman NH, Rudolph AM. Doppler echocardiographic assessment of fetal descending aortic and umbilical blood flows. Validation studies in fetal lambs. Circulation 1991;83:1731-7.
Armstrong L, Stenson BJ. Use of umbilical cord blood gas analysis in the assessment of the newborn. Arch Dis Child Fetal Neonatal Ed. 2007 Nov; 92: 430-4.
Martin JA, Hamilton BE, Ventura SJ, Osterman MJ, Wilson EC, Mathews TJ, et al.
Births: Final data for 2010. Natl Vital Stat Rep 2012;61:1-72.
Alfirevic Z, Stampalija T, Medley N. Fetal and umbilical Doppler ultrasound in normal pregnancy. Cochrane Database Syst Rev 2015;4:CD001450.
Stampalija T, Gyte GM, Alfirevic Z. Utero-placental Doppler ultrasound for improving pregnancy outcome. Cochrane Database Syst Rev 2010;9:CD008363.
Akolekar R, Syngelaki A, Gallo DM, Poon LC, Nicolaides KH. Umbilical and fetal middle cerebral artery Doppler at 35-37 weeks' gestation in the prediction of adverse perinatal outcome. Ultrasound Obstet Gynecol 2015;46:82-92.
Chalubinski KM, Repa A, Stammler-Safar M, Ott J. Impact of Doppler sonography on intrauterine management and neonatal outcome in preterm fetuses with intrauterine growth restriction. Ultrasound Obstet Gynecol 2012;39:293-8.
Shahinaj R, Manoku N, Kroi E, Tasha I. The value of the middle cerebral to umbilical artery Doppler ratio in the prediction of neonatal outcome in patient with preeclampsia and gestational hypertension. J Prenat Med 2010;4:17-21.
Bakalis S, Akolekar R, Gallo DM, Poon LC, Nicolaides KH. Umbilical and fetal middle cerebral artery Doppler at 30-34 weeks' gestation in the prediction of adverse perinatal outcome. Ultrasound Obstet Gynecol 2015;45:409-20.
Aranyosi J. Fetal aortic-cerebral Doppler resistance index ratio: An indicator of physiologic blood flow distribution. DSJUOG; 2009;3:91-5.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7]
[Table 1], [Table 2], [Table 3], [Table 4]