Utility of Doppler parameters at 36–42 weeks’ gestation in the prediction of adverse perinatal outcomes in appropriate-for-gestational-age fetuses

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VOLUME 18 , ISSUE 72 (May 2018) > List of articles

Utility of Doppler parameters at 36–42 weeks’ gestation in the prediction of adverse perinatal outcomes in appropriate-for-gestational-age fetuses

Michał Migda / Katarzyna Gieryn / Bartosz Migda / Marian Stanisław Migda / Marek Maleńczyk

Keywords : third trimester screening, middle cerebral artery Doppler, umbilical artery Doppler, appropriate-for-gestational-age

Citation Information : Journal of Ultrasonography. Volume 18, Issue 72, Pages 22-28, DOI: https://doi.org/10.15557/JoU.2018.0004

License : (OPEN-ACCESS)

Received Date : 04-December-2017 / Accepted: 07-February-2018 / Published Online: 30-March-2018

ARTICLE

ABSTRACT

Aim

To investigate the potential value of Doppler ultrasound and to assess cerebroplacental ratio (CPR) in the prediction of adverse perinatal outcome defined as Apgar score < 7 at 1 minute.

Material and methods

This was a retrospective cross-sectional study in selected pregnant women undergoing an ultrasound examination between 36 and 42 weeks of gestation. We measured estimated fetal weight (EFW), mean umbilical artery pulsatility index (UA PI), mean middle cerebral artery pulsatility index (MCA PI), CPR, and Apgar score in 1 minute. Multiples of medians (MoM) were calculated for MCA PI and UA PI.

Results

The study group consisted of 446 women, 236 were primipara and 210 were multipara. The average age was 29.6 years (range 16–46 years). The average week of delivery is 39.5 weeks of gestation (range 36–42). Mean MCA PI and UA PI were 1.3 (0.1–2.45) and 0.8 (0.39–1.66), respectively. The mean values were 1.03 (0.1–1.9) for MCA PI MoM and 1.04 (0.5–2.1) for UA PI MoM. Primiparas had lower values of MCA PI (1.27 vs. 1.34), MCA PI MoM (1.00 vs. 1.05), CPR (1.62 vs. 1.73), EFW (3479.53 g vs. 3579.25 g) and birth weight (3513.50 g vs. 3617.79 g). For CPR cut-off point of 1.08: sensitivity was (0.945), specificity 0.1, positive predictive values 0.979, negative predictive values 0.04 and accuracy 0.926. The ROC curves for CPR were: area under the curve was 0.52 at CI 95% (0.342–0.698), p = 0.8271.

Conclusion

Screening in pregnancies with appropriate-for-gestational-age fetuses at 36–42 weeks of gestation using Doppler parameters is not useful in the prediction of adverse perinatal outcomes like an Apgar score < 7 at 1 minute.

Graphical ABSTRACT

Introduction

Doppler ultrasound(1) is used to assess the flow in umbilical artery (UA) and fetal middle cerebral artery (MCA). The pulsatility index (PI) is used to calculate the cerebroplacental ratio (CPR), which is used for the assessment of fetal oxygenation(23). Abnormal Doppler findings in the third trimester are typically associated with adverse perinatal outcome(46). Most studies on the clinical use of Doppler and CPR have been focused on the assessment of small-for-gestational-age(7) fetuses, who are at increased risk for adverse perinatal outcomes and long-term neurodevelopmental impairment(811). However, a large study of Bakalis et al. regarding singleton pregnancies at 30–34 weeks of gestation reports that the majority of cases for each type of adverse perinatal outcomes concerned fetuses that were appropriate-for-gestational-age (AGA). For instance, 70% of stillbirths and 80% of cesarean sections for fetal distress occur in AGA group(12). Consequently, prenatal care should identify hypoxemic rather than small fetuses, and screen for low CPR regardless of the fetal size(5,13). It was also reported that the prediction of an adverse perinatal outcome by low CPR was better if the time interval between assessment and delivery was ≤ 2 weeks and that the screening by CPR at 36 weeks may be more valuable than at 32 weeks(2,12,14).

The objective of this study has been to investigate the usefulness of Doppler parameters obtained in third-trimester AGA fetuses for the prediction of adverse perinatal outcomes.

Material and methods

We performed a retrospective cross-sectional study between January 2012 and December 2013 in a group of pregnant women with appropriate-for-gestational-age fetuses, undergoing a routine third-trimester ultrasound examination between 36 and 42 weeks of gestation. The study was approved with an institutional review board consent of the Obstetrics, Women’s Disease and Gynecological Oncology Teaching Department, Voivodeship Hospital Complex, Collegium Medicum of the Nicolaus Copernicus University in Toruń, Poland. All the exams were performed at our Department by accredited examiners using Voluson GE E 6 (General Electric, Zipf, Austria). The inclusion criteria for this study were as follows: singleton pregnancy, gestational age determined by last menstrual period (LMP) and confirmed with crown-rump length measurement at 11–13 weeks, absence of fetal structural malformation or a genetic condition confirmed either pre- or post-natally, ultrasound examination performed no further than 2 weeks before delivery. All pregnant women included in the study were Caucasian, conception was spontaneous, were non-smokers and had no medical history of chronic hypertension, diabetes mellitus, systemic lupus erythematosus (SLE) or antiphospholipid syndrome (APS). The following ultrasound parameters were assessed: estimated fetal weight (EFW) calculated automatically using Hadlock’s formula, mean UA PI, mean MCA PI, CPR was calculated dividing MCA PI by UA PI. Doppler measurement of UA and MCA was performed according to ISUOG (International Society of Ultrasound in Obstetrics and Gynecology) guidelines. For UA Doppler, a free loop measurement was performed, with an insonation angle of <200 (Fig. 1).

Fig. 1

Doppler assessment of pulsatility index (PI) in umbilical artery (UA)

JoU-2018-0004-g001.jpg

The proper technique of MCA Doppler measurement was as follows(15):

  1. Axial section of the brain (including thalami and sphenoid wings) and magnified.

  2. Color flow mapping should be used to identify the circle of Willis and the proximal MCA (Fig. 2).

  3. The pulse-wave Doppler gate should then be placed at the proximal third of the MCA, close to the origin in the carotid artery.

  4. The angle between the ultrasound beam and the direction of blood flow should be kept as close as possible to 00 (Fig. 2).

  5. At least three to 10 consecutive waveforms should be recorded.

  6. PI is usually calculated using autotrace measurement.

We defined adverse perinatal outcomes as Apgar score of < 7 at 1 minute. In cases where the same pregnant women underwent repeated ultrasound examinations, we took into account the last exam before delivery. We did not analyze umbilical cord pH after delivery, due to the fact that our group consisted of low-risk pregnancies. Moreover, the mode of delivery was assessed with special attention to fetal distress as an indication for operational delivery (vacuum, forceps, cesarean section).

Fig. 2

Doppler assessment of pulsatility index (PI) in middle cerebral artery (MCA)

JoU-2018-0004-g002.jpg

Statistical analysis

Statistical analysis of the obtained data was performed using Statistica 10 software (StatSoft.Inc). Continuous variables were predominant: mother age, gestational age, UA PI, UA PI MoM, MCA PI, MCA PI MoM, CPR, EFW on ultrasound (US), birth weight. In addition, there was a single qualitative variable: mode of delivery.

The W-Shapiro-Wilk test was used to evaluate the normal distribution of continuous variables. The Mann-Whitney U test and Student’s t-test were used to compare continuous variables according to the distribution of data. ROC curves were used to determine the suitability of CPR as an Apgar score predictor, giving the area under the curve (AUC) with 95% confidence interval and a significance level. For measurable variables, the average, median, minimum, maximum and standard deviation were calculated. In addition, plots for UA PI and MCA PI were plotted against gestation age expressed at 95% confidence intervals.

For all calculations, p < 0.05 was considered as the statistical significance level.

Results

The study group consisted of 446 pregnant women, of which 236 were primiparas and 210 were multiparas. The average age was 29.6 years (range 16–46 years). The average age of primiparas was 27.7 years (range 16–41 years) and of multiparas 31.7 years (range 19– 46 years).

Table 1 shows the characteristics of the whole group. The average week of delivery was 39.5 weeks of gestation (range 36–42). The mean values of MCA PI and UA PI were 1.3 (0.1–2.45) and 0.8 (0.39–1.66), respectively. The mean values based on multiple of medians were 1.03 (0.1–1.9) for MCA PI MoM and 1.04 (0.5–2.1) for UA PI MoM (Tab. 1).

Tab. 1

Maternal and obstetric characteristics of the study population

Age (years)Descriptive statistics
NMeanMedianMin.Max.Lower QuartileUpper QuartileSD
Mother age44629.630164627335.044
Gestational age44639.540364239411.420
MCA PI4461.301.270.102.451.091.500.306
MCA PI MoM4461.031.000.101.900.901.200.242
UA PI4460.800.780.391.660.690.900.159
UA PI MoM4461.041.000.502.100.901.200.206
CPR4461.671.620.163.871.391.900.472
EFW USG4463526.4835532230468032003860457.060
Birth weight4463562.6135502700448032503860412.195

N – number of cases; SD – standard deviation. MCA – middle cerebral artery. UA – umbilical artery. PI – pulsatility index. CPR – cerebroplacental ratio. EFW – estimated fetal weight. US – ultrasound. MoM – multiple of medians

Seventy women were at least 35 years of age. None of the tested fetal parameters was found to be significantly different between the groups of women more and less than 35 years of age (Tab. 2).

Tab. 2

Statistical analysis of two groups <35 and ≥ 35 years old

Age (years)NMeanMin.Max.SDP
<35>35<35>35<35>35<35>35<35>35
Mother age3767028.137.6163534463.8802.4410.0000
Gestational age3767039.539.3363642421.4311.3530.0942
MCA PI376701.291.340.100.572.452.160.2990.3420.2150*
MCA PI MoM376701.021.060.100.401.901.700.2350. 740.1734
UA PI376700.800.800.390.441.661.140.1600.1570.9694
UA PI MoM376701.041.030.500.602.101.500.2070.2000.9521
CPR376701.661.740.160.533.873.510.4630.5160.3084
EFW US376703523.93540.392230250046804525458.578451.8260.7820*
Birth weight376703564.63552.142700271044804330414.126404.4350.8174*

N – number of cases; Std. – standard deviation; p* – t-Student test; p – U Mann-Whitney test, MCA – middle cerebral artery, UA – umbilical artery, PI – pulsatility index, CPR – cerebroplacental ratio, EFW – estimated fetal weight, US – ultrasound, MoM – multiple of medians

When compared to multiparas, primiparas had lower values of MCA PI (1.27 vs. 1.34), MCA PI MoM (1.00 vs. 1.05), CPR (1.62 vs. 1.73), EFW USG (3479.53 g vs 3579.25 g) and birth weight (3513.50 g vs. 3617.79 g) (Tab. 3).

Tab. 3

Statistical analysis of two groups of patients: primiparas vs multiparas

Parity (0 = primipara; 1 = multipara)NMeanMin.Max.SDP
0101010101
Mother age23621027.731.7161941464.6444.6330.0000
Gestational age23621039.539.4363642421.4681.3660.3477
MCA PI2362101.271.340.100.572.052.450.2980.3110.0119*
MCA PI MoM2362101.001.050.100.401.601.900.2330.2490.0432
UA PI2362100.800.800.490.391.451.660.1520.1670.9574
UA PI MoM2362101.041.040.600.501.902.100.1990.2140.9504
CPR2362101.621.730.160.532.993.870.4370.5030.0354
EFW US2362103479.533579.252330223046134680471.895434.8800.0213*
Birth weight2362103513.503617.792700271044704480429.786385.0750.0075*

N – number of cases; Std. – standard deviation; p*– t-Student test; p – U Mann-Whitney test, MCA – middle cerebral artery, UA – umbilical artery, PI – pulsatility index, CPR – cerebroplacental ratio, EFW – estimated fetal weight, US – ultrasound, MoM – multiple of medians

None of the parameters tested (mother age, MCA PI, MCA PI MoM, UA PI, UA PI MoM, CPR, EFW USG, birth weight) showed a difference across the groups with respect to Apgar score, or the method of delivery (Tab. 4 and Tab. 5). In our study, we used the cut-off point of 1.08, and we report a high sensitivity (0.945) but a low specificity (0.1), positive predictive values (PPV) 0.979, negative predictive values (NPV) 0.04 and accuracy (ACC) 0.926.

Tab. 4

Statistical analysis of two groups of patients that deliver a fetus with: <= 7 Apgar vs >7 Apgar

ApgarNMeanMin.Max.SDP
≤7>7≤7>7≤7>7≤7>7≤7>7
Mother age1043629.629.6251635462.8755.0850.9921
Gestational age1043640.039.5383641421.2471.4230.2476
MCA PI104361.291.301.010.101.902.450.2850.3070.9347
MCA PI MoM104361.021.030.800.101.501.900.2250.2420.7992
UA PI104360.800.800.630.390.981.660.1200.1600.8934
UA PI MoM104361.041.040.800.501.302.100.1650.2070.8165
CPR104361.671.671.050.162.973.870.5310.4710.8310
EFW USG104363618.803524.372650223043304680485.323456.7630.5189
Birth weight104363445.003565.302810270039504480393.340412.6560.3621

N – number of cases; Std.-standard deviation; p* – t-Student test; p – U Mann-Whitney test, MCA – middle cerebral artery, UA – umbilical artery, PI – pulsatility index, CPR – cerebroplacental ratio, EFW – estimated fetal weight, US – ultrasound, MoM – multiple of medians

Tab. 5

Statistical analysis of two groups of patients according to mode of delivery

Mode of deliveryNMeanMin.Max.SDP
NDOPNDOPNDOPNDOPNDOP
Mother age27317329.230.2161742464.8905.2370.1252
Gestational age27317339.639.3363642421.3711.4810.0390
MCA PI2731731.291.310.100.602.452.160.3090.3030.5002
MCA PI MoM2731731.021.030.100.501.901.700.2440.2390.8431
UA PI2731730.800.800.390.491.661.450.1670.1460.9645
UA PI MoM2731731.031.040.500.602.101.900.2150.1900.6633
CPR2731731.671.680.160.613.873.510.4920.4390.6156
EFW US2731733505.193560.082230233045264680461.068449.9380.2169
Birth weight2731733539.243599.482700270044604480414.982406.2180.1328

N – number of cases; ND – natural delivery; Op – operational delivery; SD. – standard deviation; p* – t-Student test; p – U Mann-Whitney test, MCA – middle cerebral artery, UA – umbilical artery, PI – pulsatility index, CPR – cerebroplacental ratio, EFW – estimated fetal weight, US – ultrasound, MoM – multiple of medians

The results for the analysis of ROC curves for CPR were: AUC was 0.52 at CI 95% (0.342–0.698), p = 0.8271 (Fig. 3). Figures 4 and 5 show the relationships between UA PI and MCA PI and gestational age in weeks with a 95% confidence interval.

Fig. 3

ROC curve for the cerebroplacental ratio (CPR)

JoU-2018-0004-g003.jpg
Fig. 4

Relationship between UA PI and gestational age in weeks with a 95% confidence interval

JoU-2018-0004-g004.jpg
Fig. 5

Relationship between MCA PI and gestational age in weeks with a 95% confidence interval

JoU-2018-0004-g005.jpg

Discussion

In our study, we have assessed the utility of Doppler parameters as predictors of adverse perinatal outcomes in selected groups of pregnancies with AGA fetuses in the third trimester of pregnancy. CPR is more predictive of adverse perinatal outcomes compared to a single Doppler measurement like UA PI or MCA PI(1). Grammellini et al., as well as other researchers, report that CPR values are constant throughout the last ten weeks of pregnancy, and have established a value of 1.08 as a cut-off point, beyond which (<1.08) the ratio is regarded as abnormal(8). Other authors suggest a value of CPR <1.05 to be a good predictor of an adverse perinatal outcome, but included high-risk pregnancies, e.g. complicated with arterial hypertension or gestational diabetes(16). It is of paramount importance to properly define the MCA and UA PI values as normal or abnormal, since such parameters are to reflect placental insufficiency, especially in prolonged pregnancies between 41 and 42 + 6 weeks, where perinatal morbidity and mortality increase due to frequently postulated placental obsolescence(17). Even in uncomplicated pregnancies with no symptoms of abnormal placental function, an adaptive mechanism of brain-sparing effect is activated to protect the brain throughout the adverse conditions manifested as decrease of MCA PI values even before UA alterations appear(1). In our study, we demonstrate that during the third trimester of pregnancy, MCA PI and UA PI decrease with gestational age. Such findings are similar to results presented in previous studies(7,1819). However, we found none of the analyzed Doppler parameters to be statistically significant in the prediction of adverse perinatal outcomes. In our opinion, this could have been expected, as we examined a low-risk pregnancy population. Our data are similar to Korbelak et al., who also report a low prediction rate of UA PI in predicting adverse perinatal outcomes in a low-risk population group(20). Yet, a major weakness of their study is a relatively small group of only 24 patients that were enrolled to the cohort. Recent studies, in contrast, investigate the power of Doppler parameters in predicting adverse perinatal outcomes using non-selected groups of patients, where the included complications, like small gestational age (SGA), fetal growth restriction (FGR), gestational hypertension or gestational diabetes mellitus, could influence significantly the results(2,9,12,14,16,18,2123). In our study, we found no significant correlation of Doppler parameters with Apgar score < 7 at 1 min. Yet, we report that nulliparous women, compared to multiparas, had significantly lower values of: age, MCA PI, MCA PI MoM, CPR, EFW and fetal birth weight. In our population, there was a significantly higher number of patients younger than 35 years. Natural delivery was more frequent than operational delivery, and all were emergency cesarean sections. Our results contrast with those in a study by Valino et al., where half of the cases had elective cesarean section due to a maternal or fetal condition(24).

Our study had some limitations. Firstly, it was a retrospective study. Secondly, it was a relatively small cohort of one center-based study, with a small number of Apgar score < 7 cases. The strong side of the study is the homogeneity of population of Caucasian women without risk factors and the fact that examinations were performed within a short period of time before delivery by experts trained in Doppler examinations.

Screening in pregnancies with AGA at 36–42 weeks of gestation using Doppler parameters is not useful in the prediction of adverse perinatal outcomes like an Apgar score < 7 at 1 minute.

Conflict of interest

Authors do not report any financial or personal connections with other persons or organizations that might negatively affect the contents of this publication and/or claim authorship rights thereto.

References


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  2. 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
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  3. Prior T,Mullins E,Bennett P,Kumar S,Prediction of intrapartum fetal compromise using the cerebroumbilical ratio: a prospective observational study Am J Obstet Gynecol 2013 208 124.e1 124.e6
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  4. Shwarzman P,Waintraub AY,Frieger M,Bashiri A,Mazor M,Hershkovitz R,Third-trimester abnormal uterine artery Doppler findings are associated with adverse pregnancy outcomes J Ultrasound Med 2013 32 2107 2113
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  5. Khalil AA,Morales-Rosello J,Elsaddig M,Khan N,Papageorghiou A,Bhide A,The association between fetal Doppler and admission to neonatal unit at term Am J Obstet Gynecol 2015 213 57.e1 57.e7
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  6. Khalil AA,Morales-Rosello J,Morlando M,Hannan H,Bhide A,Papageorghiou A,Is fetal cerebroplacental ratio an independent predictor of intrapartum fetal compromise and neonatal unit admission? Am J Obstet Gynecol 2015 213 54.e1 54.e10
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  11. Kwon JY,Kwon HS,Kim YH,Park YW,Abnormal Doppler velocimetry is related to adverse perinatal outcome for borderline amniotic fluid index during third trimester J Obstet Gynaecol Res 2006 32 545 549
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  12. 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 45 409 420
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  13. Prior T,Mullins E,Bennett P,Kumar S,Influence of parity on fetal hemodynamics and amniotic fluid volume at term Ultrasound Obstet Gynecol 2014 44 688 692
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FIGURES & TABLES

Fig. 1

Doppler assessment of pulsatility index (PI) in umbilical artery (UA)

Full Size   |   Slide (.pptx)

Fig. 2

Doppler assessment of pulsatility index (PI) in middle cerebral artery (MCA)

Full Size   |   Slide (.pptx)

Fig. 3

ROC curve for the cerebroplacental ratio (CPR)

Full Size   |   Slide (.pptx)

Fig. 4

Relationship between UA PI and gestational age in weeks with a 95% confidence interval

Full Size   |   Slide (.pptx)

Fig. 5

Relationship between MCA PI and gestational age in weeks with a 95% confidence interval

Full Size   |   Slide (.pptx)

REFERENCES

  1. Ropacka-Lesiak M,Korbelak T,Świder-Musielak J,Breborowicz G,Cerebroplacental ratio in prediction of adverse perinatal outcome and fetal heart rate disturbances in uncomplicated pregnancy at 40 weeks and beyond Arch Med Sci 2015 11 142 148
    [CROSSREF]
  2. 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
    [CROSSREF]
  3. Prior T,Mullins E,Bennett P,Kumar S,Prediction of intrapartum fetal compromise using the cerebroumbilical ratio: a prospective observational study Am J Obstet Gynecol 2013 208 124.e1 124.e6
    [CROSSREF]
  4. Shwarzman P,Waintraub AY,Frieger M,Bashiri A,Mazor M,Hershkovitz R,Third-trimester abnormal uterine artery Doppler findings are associated with adverse pregnancy outcomes J Ultrasound Med 2013 32 2107 2113
    [CROSSREF]
  5. Khalil AA,Morales-Rosello J,Elsaddig M,Khan N,Papageorghiou A,Bhide A,The association between fetal Doppler and admission to neonatal unit at term Am J Obstet Gynecol 2015 213 57.e1 57.e7
    [CROSSREF]
  6. Khalil AA,Morales-Rosello J,Morlando M,Hannan H,Bhide A,Papageorghiou A,Is fetal cerebroplacental ratio an independent predictor of intrapartum fetal compromise and neonatal unit admission? Am J Obstet Gynecol 2015 213 54.e1 54.e10
    [CROSSREF]
  7. Acharya G,Wilsgaard T,Berntsen GK,Maltau JM,Kiserud T,Reference ranges for serial measurements of blood velocity and pulsatility index at the intra-abdominal portion, and fetal and placental ends of the umbilical artery Ultrasound Obstet Gynecol 2005 26 162 169
    [CROSSREF]
  8. Gramellini D,Folli MC,Raboni S,Vadora E,Merialdi A,Cerebral-umbilical Doppler ratio as a predictor of adverse perinatal outcome Obstet Gynecol 1992 79 416 420
    [CROSSREF]
  9. Cruz-Martínez R,Figueras F,Hernandez-Andrade E,Oros D,Gratacos E,Fetal brain Doppler to predict cesarean delivery for nonreassuring fetal status in term small-for-gestational-age fetuses Obstet Gynecol 2011 117 618 626
    [CROSSREF]
  10. Valiño N,Giunta G,Gallo DM,Akolekar R,Nicolaides KH,Biophysical and biochemical markers at 30–34 weeks’ gestation in the prediction of adverse perinatal outcome Ultrasound Obstet Gynecol 2016 47 194 202
    [CROSSREF]
  11. Kwon JY,Kwon HS,Kim YH,Park YW,Abnormal Doppler velocimetry is related to adverse perinatal outcome for borderline amniotic fluid index during third trimester J Obstet Gynaecol Res 2006 32 545 549
    [CROSSREF]
  12. 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 45 409 420
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