|Year : 2015 | Volume
| Issue : 4 | Page : 222-229
Integration of umbilical venous and arterial Doppler flow parameters for prediction of adverse perinatal outcome
Hebbar Shripad, Rubeena Zainab, Adiga Prashant, Rai Lavanya
Department of Obstetrics and Gynaecology, Kasturba Medical College, Manipal University, Udupi, Karnataka, India
|Date of Web Publication||20-Oct-2015|
Department of Obstetrics and Gynaecology, Kasturba Medical College, Manipal University, Udupi - 576 104, Karnataka
Source of Support: None, Conflict of Interest: None
Background: Quantification of umbilical vein (UV) blood flow rate and umbilical artery Doppler indices might be valuable in assessing fetuses at increased risk of perinatal complications as they receive their supply of oxygen and nutrients through this vessel. Previous studies have indicated that UV blood volume flow rate to umbilical artery pulsatility index (UAPI) ratio (venous arterial index [VAI]) evaluates both venous and arterial arm of fetal umbilical circulation and hence, can be adopted as a screening tool in management of high risk pregnancy. Objectives: To compare umbilical VAI with adverse perinatal outcome and also to evaluate its efficacy with other flow indices in determining perinatal outcome. Materials and Methods: Various Doppler indices such as normalized blood flow rate in UV (nUV, ml/kg estimated fetal weight/min), VAI (nUV/UAPI), umbilical artery resistance index (RI), UAPI, and systolic diastolic ratio were determined in 103 pregnant women within 2 weeks of the delivery. A risk score was devised using APGAR at 5 min, birth weight, preterm delivery, fetal distress, Neonatal Intensive Care Unit (NICU) care, and perinatal death and this score was correlated with antenatal Doppler findings. Results: Subjects with low VAI were found to have a greater association with intrauterine growth restricted fetuses (28.5%) and low liquor (35.7%), preterm deliveries (46.4%), lower mean birth weight (2.25 kg), higher NICU admission rates (32.1%). The unfavorable score was noticed in 25.2% of the neonates. They had lower VAI (156 vs. 241), UV diameter (6.2 mm vs. 7.8 mm), UV velocity (16.2 vs. 17.8), nUV (163.7 vs. 206.4), and higher PI (1.3 vs. 0.9). A cut-off of VAI of 105 ml/kg/min had sensitivity of 86.7% and a specificity of 93.5% for predicting poor perinatal outcome. Conclusion: VAI with a cut-off of 105 ml/kg/min can be used as an additional tool along with the other conventional Doppler indices in order to predict adverse fetal outcome.
Keywords: Normalized umbilical venous flow, umbilical vein diameter, umbilical vein velocity, venous arterial index
|How to cite this article:|
Shripad H, Zainab R, Prashant A, Lavanya R. Integration of umbilical venous and arterial Doppler flow parameters for prediction of adverse perinatal outcome. Int J Health Allied Sci 2015;4:222-9
|How to cite this URL:|
Shripad H, Zainab R, Prashant A, Lavanya R. Integration of umbilical venous and arterial Doppler flow parameters for prediction of adverse perinatal outcome. Int J Health Allied Sci [serial online] 2015 [cited 2022 May 16];4:222-9. Available from: https://www.ijhas.in/text.asp?2015/4/4/222/167656
| Introduction|| |
Doppler investigations of the umbilical arteries have provided information regarding fetoplacental circulation. The most widely employed indices for arterial flow are the systolic diastolic ratio (S/D ratio), the resistive index (RI), and the pulsatility index (PI). A fall in end diastolic velocity elevates each of the indices and usually indicates increased downstream resistance., However, there is paucity of literature when it comes to quantification of venous Doppler flow dynamics in compromised fetoplacental circulation. Few studies have focused on the umbilical vein (UV) as a potential indicator of determining adverse perinatal outcome as it is the blood flow and not the velocimetry which determines oxygen delivery to the fetal tissues.,
Recently, evidences have shown that variations in UV blood flow significantly correlates with fetal weight.,,
Measurement of UV volume blood flow might be valuable in assessing fetuses at increased risk of developing perinatal complications as they receive their supply of oxygen and nutrients via this vessel., As the UV is a single vessel, it is reasonable to assume that blood flow could be measured at any site along its length. Absolute UV blood flow increases as a function of gestational age and it is strongly correlated with UV diameter (UvD)., Gill et al. reported that a reduction in the UV blood flow might be present up to 3 weeks before the fetal growth failure is detectable by conventional biometric measurements. Ferrazzi et al. have reported that UV blood flow is significantly reduced in intrauterine growth restricted (IUGR) fetuses as they noted a relationship between UV blood flow and the degree of fetal compromise.
Advances in Doppler technology have enabled us to quantify flow studies in the umbilical vessels and now it is possible to measure cross-sectional area of UV, flow velocity, and umbilical arterial indices such as S/D ratio, PI, and resistance index (RI) in a matter of 5 min. Many studies in the past aimed at detection of either venous or arterial arm of umbilical circulation and mostly before the occurrence of terminal events.,, IUGR, occurring late in gestation with slightly deranged Doppler parameters, in the absence of fetal or maternal diseases, represents a distinct group of fetuses with a low but not negligible risk of perinatal complications. They may have subtle changes in the circulation as manifested by reduced UV blood flow or increased umbilical artery resistance or combination of both. On the contrary, a well-nourished fetus is likely to have good venous flow and normal arterial Doppler. We presumed that by incorporating venous flow in numerator and vascular resistance in denominator may concretely predict adverse perinatal outcome as this ratio is sensitive to changes in venous and arterial circulation and this hypothesis forms the basis of the present study.
| Materials and Methods|| |
This prospective study was done in a Tertiary Maternal Unit of Kasturba Medical College, Manipal over a period of 3 years between 2011 and 2013. This center serves as a referral unit for high risk pregnancies for surrounding four districts (Dakshina Kannada, Davanagere, Shimoga, Uttara Kannada, Udupi, and Chikmagalur with a 95,40,390 population). Prior to the recruitment of subjects, informed consent was taken and Institutional Ethical Committee gave permission to conduct the study. Inclusion criteria included accurate last menstrual period confirming with thefirst trimester crown rump length measurements, upper segment placenta with recent Doppler study done within 2 weeks range from the actual date of delivery. Pregnancies with multiple gestation, congenitally malformed fetuses, intrauterine death, and placental abnormalities such as placenta previa, abruption placenta, and other ultrasonologically detectable placental malformations such as circumvallate placenta as these abnormalities may alter umbilical circulation. Pregnancies complicated by preeclampsia, IUGR, preterm labor were not considered as contraindications for patient recruitment. Detailed umbilical venous and arterial Doppler examination was carried out in 103 singleton pregnancies within 2 weeks of delivery using the Philips HD11XE ultrasound equipment with fetus in resting position as much as possible as fetal gross and respiratory movements are known to alter venous flow. As the study was still experimental, the obstetric decisions for management of pregnancy and mode of delivery were not solely influenced by the results of Doppler parameters in recruited subjects. Sample size indicated that the number of subjects studied was more than adequate to draw statistically significant derivations.
Sample size estimation
Tchirikov et al., compared UV flow volume in fetuses with normal (n = 148) and adverse perinatal outcomes (n = 33). They found that the mean value of UV flow volume (ml/min) in the control group was 253.3 ± 186.6 and the same value for the compromised group was 160.2 ± 75.4 (ml/min). Pooled variance (σ2) was calculated using the formula;
We calculated the desired sample size based on these assumptions so that we could achieve 90% power and 0.05.
Where zα = 1.96 (critical value that divides the central 95% of z distribution from 5% in the tails),
zβ = 1.28 (critical value that separates the lower 10% of distribution from upper 90%),
σ2 = pooled variance (29611.2), Δμ= required difference in mean for significant difference (253.3–160.2 = 93.1).
Accordingly, a minimum sample size of 72 patients was required and the number of patients in our study was more than adequate for hypothesis testing.
Ultrasound examination included a detailed account of fetal biometric parameters (BPD - biparietal diameter, HC - head circumference, AC - abdominal circumference, and FL - femur length), placental position, amniotic fluid index which were measured in 2D mode using 3.5 MHz abdominal probe according to standard protocol. The inbuilt software gave the estimated fetal weight using Hadlock model.
Doppler mode was used to compute various venous and arterial indices. We evaluated a new venous to arterial Doppler ratio called venous arterial index (VAI) as described by Tchirikov et al.
Following Doppler parameters were required to calculate VAI
- Diameter of intra-abdominal portion of UV (mm)
- Averaged mean velocity (AMV) of venous blood flow through the UV (cm/s)
- Estimated fetal weight
- PI of the umbilical artery.
Umbilical vein diameter
A straight segment of the intra-abdominal part of the UV was chosen and Doppler gate was positioned to completely cover the vessel's diameter. The approximate vessel diameter were determined (in cm) using a longitudinal section of the UV in real-time mode following the "maximum principle" of ultrasound physics [Figure 1], [Figure 2], [Figure 3]. This includes the measurement of the maximal vessel diameter to the nearest tenth of a millimeter by placing the calipers at right angles to the vessel axis on a frozen B-mode image [Figure 4]. The angle of insonation was kept minimum (around 30° or less). The measurements were taken 3 times and then averaged.
|Figure 1: Maximum principle. Ultrasound beam cuts the vessel parallel and exactly through the mid portion of the vessel. Both the diameter and flow velocity are maximum in this slice. The rectangular grid shows the vessel area where the ultrasound beam passes through|
Click here to view
|Figure 2: The ultrasound beam cuts the vessel parallel but at the edge. The rectangular grid shows the vessel area where the ultrasound beam passes through. The vessel diameter is less this in cut section, though flow velocity may remain the same. This plane should be avoided|
Click here to view
|Figure 3: Ultrasound beam cuts the vessel obliquely. Maximum vessel diameter may not be affected, but the flow velocity is reduced. The elliptical grid shows the vessel area where the ultrasound beam passes through. Again this plane should be avoided|
Click here to view
|Figure 4: Ultrasound image showing measurement of intra-abdominal portion of umbilical vein|
Click here to view
Averaged mean velocity of venous blood flow (cm/min) through the umbilical vein
The ultrasound equipment automatically calculates flow velocity in cm/s after freezing the UV wave form [Figure 5]. The value was multiplied by 60 to get the velocity in cm/min.
|Figure 5: Ultrasound image showing Doppler wave form analysis of umbilical vein blood flow|
Click here to view
Estimated fetal weight
This was calculated in kilograms by measuring BPD, HC, AC, and FL and using Hadlock formula.
Pulsatility index of the umbilical artery
was calculated by performing umbilical artery Doppler wave form analysis. For this, a free loop of cord away from the placenta and anterior abdominal wall insertion was taken.
Further derivations of indices
- The UV volume flow (UVVF) was calculated from UvD and AMV as ml/min using the formula
- UV blood flow rate (UVVF) = AMV × π (UvD/2)2
- Normalized umbilical venous blood volume flow (nUV) was calculated as mL/min/kg using the formula
- nUV = UVVF/estimated fetal weight
- VAI was calculated using the formula
- VAI = nUV/PI where PI is the PI of umbilical artery.
We have taken volume measurement in cubic centimeter and time unit in minutes by using appropriate conversion factors as the ultrasound machine gives the UvD in mm and velocity in cm/s. We have nUV blood by measuring the blood flow/kg of fetal mass to nullify the effect of body weight on the quantity of flow (as small fetuses will have small blood volume, large fetuses will have large volume, but both fetuses may be receiving equal flow/kg of body weight, and in that case, both may do well within the uterus or after birth). Of three arterial indices (S/D ratio, RI and PI), we have chosen PI in denominator. The rationale is that S/D ratio can take any value one to infinity (for example, when diastolic flow gradually reduces to zero and finally becomes absent) and hence, not ideal. RI index can range between 0 and 1 and again VAI index may have wide variations. However, it can be mathematically shown that PI ratio varies between 1 and 2 (when D = S, PI = 1, and when D = 0 [minimum value of D before occurrence of reversal of flow], PI = 2) and hence, serves as a better denominator for VAI.
The outcome variables included preterm delivery rates, the occurrence of fetal distress during labor, APGAR scores at birth, birth weight, Neonatal Intensive Care Unit (NICU) admissions, and perinatal death. As said earlier, the obstetricians in charge of the patients were not aware of the Doppler measurements of umbilical circulation and hence, did not have any impact on patient care.
The analysis was performed using SPSS version 15 (SPSS Inc., Chicago, Illinois, 2006) software. Quartiles were determined using frequency distribution. Descriptive statistics was used to calculate mean, standard deviation, range, and ordinal variables were analyzed using cross tabulation. Significance of variables was determined by Pearson Chi-square test, Students t-test, and one-way ANOVA. P < 0.05 was considered significant. Receiver operator characteristic (ROC) analysis was carried out to determine the best cut-off values for various venous, arterial, and combined Doppler parameters.
| Results|| |
Umbilical venous and arterial parameters were studied in all the 103 recruited cases within 2 weeks of delivery. If the patient had ultrasound examination more than 2 weeks before delivery, the study was repeated. The median interval between Doppler study and time of delivery was 8 days (95% CI, 5–12 days). As we did not have cut-off points for ultrasound indices, we decided to divide the patients into three groups based on quartile values of VAI. We presumed that the groups having VAI values <25th percentile are likely to have compromised circulation, groups having VAI range between 25th and 75th percentile values are likely to be normal, and VAI value >75th percentile likely to present high flow group.
[Table 1] shows VAI statistics.
Thus, we could form three groups, Group 1 (n = 28), Group 2 (n = 51), and Group 3 (n = 24). The corresponding VAI values are given [Table 2].
[Table 3] shows the patient (maternal) profile and the incidence obstetrical risk factors in both groups.
There were no significant differences in maternal age, parity in any of the three groups. The period of gestation at delivery was the least for Group 1 (35 ± 3 weeks). Though not statistically significant, Group 1 which had the least VAI, was found to have a greater association with IUGR fetuses (28.5%) and low liquor (35.7%).
Various neonatal factors were also studied in these three groups [Table 4].
Group 1, which had the least VAI, was found to have a greater association with preterm deliveries (46.4%), lower mean birth weight (2.25 kg), higher NICU admission rates (32.1%). No statistical differences were found with regard to fetal distress in labor and low APGAR scores.
We also compared various other Doppler indices in these three groups. The results are shown in [Table 5].
All venous indices were reduced and arterial indices were increased in Group 1 as compared to the other groups and this was statistically significant for all the parameters except for S/D ratio.
We studied various perinatal outcomes such as preterm delivery rates, occurrence of fetal distress during labor, APGAR scores at birth, birth weight, NICU admissions, and perinatal death. As some of the adverse outcomes were observed in a single neonate, we devised a composite scoring system based on these outcomes as indicated in [Table 6]. Accordingly, 28 subjects out of 103 had poor outcome score.
We studied various Doppler indices in subjects with unfavorable and favorable findings according to [Table 6]. The results of this analysis are shown in [Table 7].
The fetuses with an unfavorable outcome (<2) had lower VAI (156 vs. 241), UVD (6.2 vs. 7.8 mm), UV velocity (UVel) (16.2 vs. 17.8 cm/s), nUV (206.4 vs. 163.7 ml/min/kg), and higher PI (1.3 vs. 0.9). We also found that mean VAI was low in fetuses with IUGR (138 vs. 241 ml/kg/min) and low liquor (144 vs. 237 ml/kg/min).
Forty (38.8%) of neonates were found to have SGA (as assigned by the pediatrician). VAI in SGA fetuses was lower than the normal weight fetuses (164 vs. 261.9). We had one intrauterine fetal demise at 26 weeks due to severe preeclampsia, oligohydramnios, and IUGR. VAI in this patient was 4.16 ml/kg/min and PI of umbilical artery was 4.16. She also had reversal of end diastolic flow.
We used 105 ml/kg/min as the cut-off for the prediction of poor perinatal outcome. From this, we got a sensitivity of 86.7% and a specificity of 93.5% for VAI [Table 8].
| Discussion|| |
Many studies in the past have tried to measure UV blood flow in a free loop of umbilical cord.,,, However, the diameter is not constant and it has been shown that the vessel caliber decreases gradually from fetus to placenta. Hence, there are varying reports of umbilical venous flow in both in normal and growth restricted fetuses., The angle of insonation of Doppler beam to the vessel may also a contributing factor, as it should be kept <30° for accurate flow estimation. Studies have shown that intra-abdominal portion of the UV is relatively stable, easily imaged in axial plane of fetal abdomen, not affected by Doppler angle.,
In the study, we have attempted to evaluate if venous blood flow/min/kg fetal weight (VAI) has any influence on the perinatal outcome. We used quartiles to determine cut-offs for VAI and compared the various outcome parameters among these quartiles to find out the value of VAI below which fetal compromise is more likely to occur.
Tchirikov et al. in their prospective study involving 181 fetuses (between 17 weeks and 41 weeks of gestation) measured various umbilical venous and arterial Doppler indices. They devised a risk score based on the umbilical cord pH, the 1 min APGAR score, birth weight, duration of gestation, type of neonatal respiratory support, and referral to the NICU. Accordingly, fetuses were assigned to a control (n = 148) or pathological group (n = 33). They reported decreased venous parameters for pathological group and increased arterial indices for control group. The pathological group had UVel 12.58 cm/s, UvD 5.17 mm, normalized UV blood flow (nUV) 115.1 ml/min/kg, UV PI 1.71, whereas the corresponding values were 15.95 cm/s, 5.45 mm, 200.3 ml/min/kg, and 1.03 in control group. From [Table 7], it can be seen that we too had similar trend, though the values slightly differed. Further, the same group of authors conducted ROC analysis to determine the best cut-off values for various Doppler indices to determine the pathological state of the fetus. They could achieve sensitivity of 69.7%, 54.5%, 51.5% for VAI, nUV, and UAPI for predicting adverse fetal outcome. The corresponding specificity rates were 90.4%, 95.9%, and 100%. They opined that a single Doppler index which they named as VAI at cut-off level of 100 ml/min/kg had the best diagnostic performance for identification of compromised fetuses. Our study too showed comparable results [Table 8] and we found that a VAI <105 ml/min/kg could be used to predict poor perinatal outcome. The sensitivity and specificity of various Doppler indices along with their cut-off values, sensitivity, and specificity are shown in detail in [Table 8].
In our study, the subjects who had VAI values between 25th and 75th percentile (Group 2) had mean UvD of 7.34 mm, blood flow velocity of 16.92 cm/s, and normalized blood flow of 173 ml/min/kg [Table 2]. Boito et al. in their study reported the corresponding values as 8.08 mm, 7.13 cm/s, and 78.3 ml/min/kg. This variation might have occurred due to different technique of measurement (extra abdominal portion of UV is used for flow study).
Our scoring system to differentiate between favorable and unfavorable fetal outcome was devised by modifying the one used by Tchirikov et al. and included the variables shown in [Table 6]. In our study, the mean birth weight in the affected fetuses was lower (2 kg) than the normal fetuses (2.8 kg). Tchirikov et al. found that in the compromised fetuses the mean birth weight was 3390 g versus 1790 g in the control group. Boito et al. had a mean weight of 1009 g versus 1247 g in the cases versus the control group. Ferrazzi et al. found a difference in birth weights in the cases (1934 g) versus control (2577 g).
In our series, NICU admission rates were higher in VAI <25th centile value (32.1% vs. 19.6%) and there was one death in thefirst VAI group [Table 7]. Tchirikov et al. too found a higher incidence of fetuses that required admission to neonatal department among the compromised group - 91% versus 29.1% in the control group.
It is well known that Doppler findings such as either absent or reversed diastolic flow in umbilical artery and pulsatile pattern in umbilical vein indicate poor foetal outcome. However, but by the time these changes are seen, the foetus is already compromised in utero and may have severe acidosis at birth. Hence these Doppler changes may be used to diagnose foetal hypoxia but not as a screening tool to predict birth asphyxia.
The parameters studied in the current article mainly serve as screening tools to identify those fetuses who are likely to have adverse outcomes before the actual hypoxic events start. Hence investigating these parameters at frequent intervals may avert a potential mishap. Though this practice may result in some degree of maternal apprehension, it is better to be cautious rather than being complacent.
The VAI may, only, become acceptable to the obstetricians if studied in the larger patient cohort. The present study may provide some useful information to other researchers in this field to initiate multicenter research and finally evidence based opinion emerges regarding the usefulness of this screening tool.
| Conclusion|| |
We have found in our study that low venous blood flow to the fetus results in greater chances of fetal compromise with subsequent IUGR, low birth weight, and neonatal complications. This is due to the reduced supply of oxygenated blood to the growing fetus which is carried by the UV. Umbilical VAI can be used as a complimentary screening tool to the routine umbilical artery Doppler studies to add more value to antenatal detection of compromised fetuses as it is a quantitative parameter as against umbilical artery Doppler parameters which are qualitative studies of fetal blood vessels.
Limitations of the study
- Though Group 1 (VAI ≤105) had higher incidence of IUGR, low liquor, preterm delivery, NICU admission rates, even other Groups (2 and 3) were not totally free from these complications. Moreover, hence, this parameter requires higher sensitivity and specificity in predicting adverse fetal outcomes precisely
- There are other Doppler parameters (such as flow patterns in umbilical vessels, ductus venosus) which are more sensitive to predict impeding fetal compromise and hence, VAI may be used only as a screening tool, but for obstetric decision making.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Battaglia C, Artini PG, Galli PA, D'Ambrogio G, Droghini F, Genazzani AR. Absent or reversed end-diastolic flow in umbilical artery and severe intrauterine growth retardation. An ominous association. Acta Obstet Gynecol Scand 1993;72:167-71.
Todros T, Ronco G, Fianchino O, Rosso S, Gabrielli S, Valsecchi L, et al.
Accuracy of the umbilical arteries Doppler flow velocity waveforms in detecting adverse perinatal outcomes in a high-risk population. Acta Obstet Gynecol Scand 1996;75:113-9.
Benson CB, Doubilet PM. Doppler criteria for intrauterine growth retardation: Predictive values. J Ultrasound Med 1988;7:655-9.
Kohl T, Silverman NH. Evaluation of umbilical venous blood flow by Doppler color flow mapping and conventional ultrasonographic methods. J Ultrasound Med 1996;15:465-73.
Haugen G, Kiserud T, Godfrey K, Crozier S, Hanson M. Portal and umbilical venous blood supply to the liver in the human fetus near term. Ultrasound Obstet Gynecol 2004;24:599-605.
Bellotti M, Pennati G, De Gasperi C, Bozzo M, Battaglia FC, Ferrazzi E. Simultaneous measurements of umbilical venous, fetal hepatic, and ductus venosus blood flow in growth-restricted human fetuses. Am J Obstet Gynecol 2004;190:1347-58.
Kaponis A, Harada T, Makrydimas G, Kiyama T, Arata K, Adonakis G, et al.
The importance of venous Doppler velocimetry for evaluation of intrauterine growth restriction. J Ultrasound Med 2011;30:529-45.
Baschat AA, Gembruch U, Harman CR. The sequence of changes in Doppler and biophysical parameters as severe fetal growth restriction worsens. Ultrasound Obstet Gynecol 2001;18:571-7.
Lackman F, Capewell V, Gagnon R, Richardson B. Fetal umbilical cord oxygen values and birth to placental weight ratio in relation to size at birth. Am J Obstet Gynecol 2001;185:674-82.
Weissman A, Jakobi P, Bronshtein M, Goldstein I. Sonographic measurements of the umbilical cord and vessels during normal pregnancies. J Ultrasound Med 1994;13:11-4.
Jouppila P, Kirkinen P, Puukka R. Correlation between umbilical vein blood flow and umbilical blood viscosity in normal and complicated pregnancies. Arch Gynecol 1986;237:191-7.
Kirkinen P, Jouppila P, Eik-Nes S. Umbilical vein blood flow in rhesus-isoimmunization. Br J Obstet Gynaecol 1983;90:640-3.
Gill RW, Kossoff G, Warren PS, Garrett WJ. Umbilical venous flow in normal and complicated pregnancy. Ultrasound Med Biol 1984;10:349-63.
Ferrazzi E, Rigano S, Bozzo M, Bellotti M, Giovannini N, Galan H, et al.
Umbilical vein blood flow in growth-restricted fetuses. Ultrasound Obstet Gynecol 2000;16:432-8.
Figueras F, Fernández S, Hernández-Andrade E, Gratacós E. Umbilical venous blood flow measurement: Accuracy and reproducibility. Ultrasound Obstet Gynecol 2008;32:587-91.
Huisman TW. Doppler assessment of the fetal venous system. Semin Perinatol 2001;25:21-31.
Najafzadeh A, Dickinson JE. Umbilical venous blood flow and its measurement in the human fetus. J Clin Ultrasound 2012;40:502-11.
Baschat AA, Gembruch U, Reiss I, Gortner L, Weiner CP, Harman CR. Relationship between arterial and venous Doppler and perinatal outcome in fetal growth restriction. Ultrasound Obstet Gynecol 2000;16:407-13.
Tchirikov M, Strohner M, Förster D, Hüneke B. A combination of umbilical artery PI and normalized blood flow volume in the umbilical vein: Venous-arterial index for the prediction of fetal outcome. Eur J Obstet Gynecol Reprod Biol 2009;142:129-33.
Hadlock FP, Harrist RB, Sharman RS, Deter RL, Park SK. Estimation of fetal weight with the use of head, body, and femur measurements – A prospective study. Am J Obstet Gynecol 1985;151:333-7.
Tchirikov M, Rybakowski C, Hüneke B, Schoder V, Schröder HJ. Umbilical vein blood volume flow rate and umbilical artery pulsatility as 'venous-arterial index' in the prediction of neonatal compromise. Ultrasound Obstet Gynecol 2002;20:580-5.
Boito S, Struijk PC, Ursem NT, Stijnen T, Wladimiroff JW. Umbilical venous volume flow in the normally developing and growth-restricted human fetus. Ultrasound Obstet Gynecol 2002;19:344-9.
Fernandez S, Figueras F, Gomez O, Martinez JM, Eixarch E, Comas M, et al.
Intra- and interobserver reliability of umbilical vein blood flow. Prenat Diagn 2008;28:999-1003.
Link G, Clark KE, Lang U. Umbilical blood flow during pregnancy: Evidence for decreasing placental perfusion. Am J Obstet Gynecol 2007;196:489.e1-7.
Li WC, Ruan XZ, Zhang HM, Zeng YJ. Biomechanical properties of different segments of human umbilical cord vein and its value for clinical application. J Biomed Mater Res B Appl Biomater 2006;76:93-7.
Yamamoto M, Carrillo J, Insunza A, Mari G, Ville Y. Error introduced into velocity measurements by inappropriate Doppler angle assignment. Ultrasound Obstet Gynecol 2006;28:853-4.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8]