Abstract
Objectives
To evaluate a novel bilateral, segment‐based umbilical artery (UA) Doppler scoring system in pregnancies complicated by early‐ or late‐onset fetal growth restriction (FGR) and to investigate its association with adverse perinatal outcome.
Methods
This single‐center prospective cohort study, conducted between May 2025 and December 2025, included singleton pregnancies diagnosed with FGR according to Delphi consensus criteria. Bilateral UA Doppler measurements were obtained from six predefined anatomical sites: the perivesical segment, the free‐loop segment and the placental insertion site in each UA. End‐diastolic flow at each site was categorized as present, absent or reversed and incorporated into a cumulative UA Doppler score (0–18 points). Composite adverse perinatal outcome (CAPO) was defined as the occurrence of at least one of the following: neonatal hypoglycemia, need for phototherapy, neonatal sepsis, respiratory distress syndrome, need for continuous positive airway pressure, need for mechanical ventilation, 5‐min Apgar score < 7 or admission to the neonatal intensive care unit (NICU). Participants were stratified by UA Doppler score (< 3 vs ≥ 3 points). Multivariable logistic regression analysis was used to assess the association between UA Doppler score as a continuous or dichotomized variable and CAPO, adjusting for maternal age, body mass index, parity, mode of conception, estimated fetal weight percentile and gestational age at delivery. In addition, the prevalence of individual markers of fetoplacental hemodynamic deterioration, including abnormal ductus venosus Doppler, cerebroplacental ratio < 5th percentile, intrauterine fetal demise, fetal distress leading to delivery and 5‐min Apgar score < 7, was analyzed across UA Doppler score categories (0–2, 3–5, 6–8, 9–12 and > 12 points).
Results
A total of 251 pregnancies with FGR were included, of which 117 were early onset (< 32 weeks' gestation) and 134 were late onset (≥ 32 weeks' gestation). Higher UA Doppler scores (≥ 3 points) were associated significantly with preterm delivery and higher rates of NICU admission and CAPO in both early‐ and late‐onset FGR. In early‐onset FGR, higher scores were associated additionally with lower birth weight. The UA Doppler score remained associated independently with CAPO on multivariable logistic regression analysis. A significant linear trend was observed across increasing UA Doppler score categories for the rate of CAPO and individual markers of fetoplacental hemodynamic deterioration.
Conclusions
In pregnancies complicated by early‐onset or late‐onset FGR, a higher UA Doppler score based on a multisite bilateral scoring system is associated independently with adverse perinatal outcome. These findings support the feasibility of a segment‐based approach to UA Doppler assessment. Further studies are required to determine the clinical benefit and feasibility of adoption within current surveillance strategies. © 2026 International Society of Ultrasound in Obstetrics and Gynecology.
Keywords: adverse perinatal outcome, Doppler scoring system, fetal growth restriction, perinatal outcome, umbilical artery Doppler
Introduction
Fetal growth restriction (FGR) refers to the failure of a fetus to reach its genetically determined growth potential in utero and affects approximately 5–10% of pregnancies 1 , 2 , 3 . The definition of FGR varies among international guidelines and expert groups 4 . The most widely accepted criteria to date, proposed by the Delphi consensus, classify FGR according to gestational age, biometric thresholds and Doppler findings 5 , 6 . FGR is categorized typically into two clinical phenotypes based on gestational age at diagnosis: early‐onset FGR, which occurs before 32 weeks' gestation, and late‐onset FGR, diagnosed at or beyond 32 weeks 6 , 7 . These two phenotypes differ not only in timing of onset but also in their clinical course. Early‐onset FGR is often linked to severe uteroplacental dysfunction and is associated with a higher risk of perinatal mortality and severe neonatal morbidity compared with late‐onset FGR, due largely to the consequences of prematurity 8 , 9 .
Doppler velocimetry plays a critical role not only in establishing the diagnosis of FGR but also in guiding ongoing prenatal surveillance and management 10 . Although umbilical artery (UA) Doppler assessment is central to FGR management, current guidelines generally recommend sampling from a single UA at the free‐loop segment for reasons of practicality 1 , 11 , 12 . This approach has been adopted widely in clinical practice due to the accessibility of the free‐loop segment of the UA during ultrasound examination, good interoperator reproducibility and perceived standardization. However, this approach inherently assumes hemodynamic uniformity both along the length of the umbilical cord and between the two UAs. In contrast, experimental and clinical studies have demonstrated consistently the presence of a longitudinal pressure gradient along the umbilical cord, with higher impedance at the perivesical segment and lower impedance toward the placental insertion, as well as meaningful interartery differences between the left and right UAs 13 , 14 . Thus, conventional free‐loop UA Doppler sampling may provide an incomplete representation of fetoplacental hemodynamics, especially in the presence of regional or interartery variability, with potential implications for diagnostic accuracy and risk stratification.
In this study, Doppler parameters from both UAs were assessed systematically across multiple cord segments to detect potential flow discordance and/or regional variation. Our objectives were to determine whether Doppler profiles differ between early‐ and late‐onset FGR and to evaluate whether bilateral multisite UA assessment improves the identification of fetuses at risk of adverse perinatal outcome. By characterizing the hemodynamic patterns and perinatal outcomes in early‐ vs late‐onset FGR, we aimed to contribute evidence that may refine risk stratification for growth‐restricted pregnancies.
Methods
Study design, participants and outcome measures
This prospective cohort study was conducted at the Perinatology Department of Ankara Etlik City Hospital, Ankara, Turkey, between May 2025 and December 2025. Pregnant women with a singleton gestation diagnosed with FGR were enrolled consecutively. FGR was defined according to the Delphi consensus criteria 6 . Per these criteria, early‐onset FGR (< 32 weeks' gestation) was defined as estimated fetal weight (EFW) < 3rd percentile, or EFW < 10th percentile together with uterine artery or UA pulsatility index (PI) > 95th percentile 6 . Late‐onset FGR (≥ 32 weeks' gestation) was defined as EFW < 3rd percentile, or EFW < 10th percentile accompanied by cerebroplacental ratio (CPR) < 5th percentile or UA‐PI > 95th percentile 6 . Exclusion criteria included multiple gestation, major fetal structural or chromosomal anomaly, intrauterine infection and maternal systemic disease, including pre‐eclampsia, chronic or gestational hypertension, and pregestational or gestational diabetes mellitus. Maternal demographic characteristics and obstetric data were recorded at enrolment and during follow‐up. All participants underwent standardized Doppler ultrasound evaluation, and follow‐up continued until delivery. Following the diagnosis of FGR, fetal biometry was repeated approximately every 2 weeks to assess interval growth. Doppler surveillance was tailored according to the severity of UA abnormality: assessments were performed at least weekly in cases with elevated PI and twice weekly in those with absent end‐diastolic flow (EDF0), while patients with reversed end‐diastolic flow (EDF−) received close inpatient monitoring 15 . Delivery timing was determined according to gestational age and the severity of UA Doppler abnormality. In late‐onset FGR with preserved end‐diastolic flow (EDF+), delivery was generally planned at 38–39 weeks' gestation, or at 36–37 weeks in cases of elevated UA‐PI or EFW < 3rd percentile. In early‐onset FGR, EDF0 prompted consideration of delivery at approximately 33–34 weeks, whereas EDF− lowered the threshold to 30–32 weeks, depending on fetal stability and overall clinical condition. Perinatal outcomes were extracted from delivery and neonatal records. The study was conducted in accordance with the Declaration of Helsinki, and ethical approval was obtained from the Ankara Etlik City Hospital Ethics Committee (approval number: AESH‐BADEK‐2024‐964). Written informed consent was obtained from all participants prior to inclusion in the study.
Composite adverse perinatal outcome (CAPO) was defined as the occurrence of at least one of the following: neonatal hypoglycemia, need for phototherapy, neonatal sepsis, respiratory distress syndrome (RDS), need for continuous positive airway pressure (CPAP), need for mechanical ventilation, 5‐min Apgar score < 7 or admission to the neonatal intensive care unit (NICU). CAPO was assessed for all participants and was used as a key clinical endpoint in subgroup and regression analyses. In addition to the composite outcome, biologically relevant markers of fetoplacental hemodynamic deterioration were evaluated individually, including absent or reversed a‐wave in the ductus venosus (DV), abnormal CPR (< 5th percentile), intrauterine fetal demise, fetal distress leading to delivery and 5‐min Apgar score < 7. CPR was calculated as middle cerebral artery (MCA) PI divided by UA‐PI derived from the free‐loop mean PI measurement. Doppler indices were interpreted according to gestational‐age‐adjusted reference standards 16 , 17 .
Data collection and ultrasound procedures
All participants underwent detailed ultrasound and Doppler examinations using a Voluson E8 system (GE Healthcare, Zipf, Austria), equipped with a 2–6‐MHz convex transducer. Examinations were performed in accordance with the recommendations of the International Society of Ultrasound in Obstetrics and Gynecology (ISUOG) 12 . Measurements were taken by a single experienced perinatologist (D.D.B.) who was blinded to clinical and outcome data. Doppler ultrasound was performed at the time of FGR diagnosis, as part of a single standardized evaluation for all participants. The examination was performed irrespective of gestational age, based on the clinical timing of diagnosis. All Doppler assessments were performed during the fetal immobility period, and at least three consecutive smooth waveforms were recorded at each site. Bilateral UA Doppler waveforms were obtained at six anatomical sites: the perivesical segment, the free loop of the umbilical cord and the placental insertion site in each UA (Figure 1). The PI value, corresponding percentile and presence of EDF0/EDF− were recorded separately for each artery and each segment. The Doppler cursor was positioned carefully within the 2–4‐mm range, and the angle of insonation was kept below 30° to ensure accuracy. MCA Doppler measurements were obtained from the proximal third of the vessel.
Figure 1.
Multisite bilateral umbilical artery Doppler evaluation demonstrating segmental heterogeneity of fetoplacental circulation: (a) right umbilical artery, placental insertion site; (b) right umbilical artery, free‐loop segment; (c) right umbilical artery, perivesical segment; (d) left umbilical artery, placental insertion site; (e) left umbilical artery, free‐loop segment; and (f) left umbilical artery, perivesical segment. Umb‐ED, umbilical artery end‐diastolic velocity; Umb‐HR, fetal heart rate; Umb‐MD, umbilical artery mean flow velocity; Umb‐PI, umbilical artery pulsatility index; Umb‐PS, umbilical artery peak systolic velocity; Umb‐RI, umbilical artery resistance index; Umb‐S/D, umbilical artery systolic/diastolic ratio; Umb‐TAmax, umbilical artery time‐averaged maximum velocity.
Modified umbilical artery Doppler scoring system
In this study, a novel segment‐based UA Doppler scoring system was developed, informed conceptually by the framework proposed by Paladini in a recent opinion article 18 . The scoring system was designed to quantify the severity and spatial distribution of fetoplacental hemodynamic compromise through systematic assessment of Doppler flow patterns at multiple anatomical sites. Specifically, EDF was evaluated at six distinct sites: the left and right perivesical segments, the left and right free‐loop segments, and the left and right placental insertion sites. At each location, EDF was categorized as present, absent or reversed, and scored according to increasing severity (Table 1). The total UA Doppler score ranged from 0 (EDF+ at all six sites) to a maximum of 18 (EDF− at all six sites), reflecting the cumulative vascular resistance across the umbilical cord. When side‐matching between segments at different sampling sites was technically unclear, vessels were aligned based on relative PI values.
Table 1.
Modified umbilical artery (UA) Doppler scoring system
| Sampling site | EDF+ | EDF0 | EDF− |
|---|---|---|---|
| Perivesical segment | |||
| Right UA | 0 | 1 | 2 |
| Left UA | 0 | 1 | 2 |
| Free loop | |||
| Right UA | 0 | 2 | 3 |
| Left UA | 0 | 2 | 3 |
| Placental insertion | |||
| Right UA | 0 | 3 | 4 |
| Left UA | 0 | 3 | 4 |
Total UA Doppler score ranges from 0 to 18. EDF+, present end‐diastolic flow; EDF0, absent end‐diastolic flow; EDF−, reversed end‐diastolic flow.
Statistical analysis
The Kolmogorov–Smirnov test was used to assess the normality of distribution for continuous variables. Data are expressed as mean ± SD for normally distributed variables. Categorical variables are presented as n (%). Comparisons between groups were performed using the independent‐samples t‐test for continuous variables and the chi‐square test or Fisher's exact test, as appropriate, for categorical variables.
For subgroup analysis, participants were stratified according to UA Doppler score (< 3 vs ≥ 3 points) within the early‐ and late‐onset FGR groups. To assess the linear trend between UA Doppler score and categorical outcomes, including CAPO and individual markers of fetoplacental hemodynamic deterioration, UA Doppler score was categorized into five groups (0–2, 3–5, 6–8, 9–12 and > 12 points) and the Cochran–Armitage test for trend was used. Multivariable logistic regression analysis was performed to identify independent predictors of CAPO and to evaluate the incremental prognostic value of the multisite UA Doppler scoring system, modeled separately as a continuous and as a dichotomized variable. Six explanatory structured models containing various UA Doppler parameters were constructed; all were adjusted for maternal age, body mass index (BMI), parity, mode of conception, EFW percentile and gestational age at delivery. Abnormal free‐loop UA Doppler was defined as UA‐PI ≥ 95th percentile and/or EDF0/EDF−. Results are reported as adjusted odds ratios (aORs) with 95% CI. Model performance was evaluated using Nagelkerke R2 and overall classification accuracy. To enhance clinical applicability, a calculator based on the proposed multisite UA Doppler scoring system and an L2‐regularized multivariable logistic regression model constructed specifically for CAPO prediction is provided in Appendix S1. Statistical analysis was performed using SPSS version 22.0 (IBM Corporation, Armonk, NY, USA). P< 0.05 was considered statistically significant.
A power analysis was performed using G*Power version 3.1.9.7 software (Heinrich Heine University Düsseldorf, Düsseldorf, Germany). Assuming a moderate effect size (Cohen's d = 0.5), a two‐sided α of 0.05 and 95% power, the minimum required total sample size was 210 participants.
Results
Baseline characteristics and perinatal outcome
A total of 251 singleton pregnancies diagnosed with FGR were included, comprising 117 early‐onset and 134 late‐onset cases. Baseline maternal characteristics, including maternal age, parity, mode of conception and BMI, were similar between groups (all P > 0.05) (Table 2). However, pregnancies with early‐onset FGR delivered significantly earlier, had lower birth weights, and were more frequently delivered preterm compared with late‐onset FGR (all P < 0.001). The rate of Cesarean delivery was significantly higher in the early‐onset group (P = 0.031). Neonatal morbidities, including hypoglycemia, need for phototherapy, sepsis, RDS, need for CPAP, need for mechanical ventilation, 5‐min Apgar score < 7 and NICU admission, were significantly more common among early‐onset FGR cases. CAPO was observed in 65.8% of early‐onset FGR cases compared with 40.3% of late‐onset FGR cases (P < 0.001).
Table 2.
Baseline maternal characteristics and obstetric and neonatal outcomes of 251 pregnancies with early‐ or late‐onset fetal growth restriction (FGR)
| Characteristic | Early‐onset FGR (n = 117) | Late‐onset FGR (n = 134) | P |
|---|---|---|---|
| Maternal age (years) | 27.4 ± 5.0 | 26.5 ± 5.4 | 0.268 |
| Nulliparous | 68 (58.1) | 81 (60.4) | 0.140 |
| Mode of conception | 0.062 | ||
| Spontaneous | 94 (80.3) | 119 (88.9) | |
| In‐vitro fertilization | 23 (19.7) | 15 (11.1) | |
| BMI at presentation (kg/m2) | 32.7 ± 11.5 | 33.8 ± 7.5 | 0.654 |
| GA at delivery (weeks) | 34.1 ± 2.6 | 37.0 ± 1.0 | < 0.001 |
| Preterm birth (< 37 weeks) | 67 (57.3) | 41 (30.6) | < 0.001 |
| Mode of delivery | 0.031 | ||
| Vaginal | 78 (66.7) | 112 (83.6) | |
| Cesarean section | 39 (33.3) | 22 (16.4) | |
| Birth weight (g) | 1932 ± 511 | 2295 ± 291 | < 0.001 |
| Fetal distress leading to delivery | 25 (21.4) | 35 (26.1) | 0.454 |
| Corticosteroid treatment | 57 (48.7) | 12 (9.0) | < 0.001 |
| Intrauterine fetal demise | 3 (2.6) | 0 (0) | 0.100 |
| Neonatal hypoglycemia | 36 (30.8) | 14 (10.4) | < 0.001 |
| Phototherapy | 24 (20.5) | 10 (7.5) | 0.003 |
| Neonatal sepsis | 7 (6.0) | 0 (0) | 0.013 |
| Transient tachypnea of the newborn | 66 (56.4) | 44 (32.8) | < 0.001 |
| Respiratory distress syndrome | 44 (37.6) | 15 (11.2) | < 0.001 |
| CPAP | 46 (39.3) | 15 (11.2) | < 0.001 |
| Mechanical ventilation | 34 (29.1) | 3 (2.2) | < 0.001 |
| 5‐min Apgar score | 8 ± 1 | 9 ± 1 | < 0.001 |
| 5‐min Apgar score < 7 | 27 (23.1) | 9 (6.7) | < 0.001 |
| NICU admission | 73 (62.4) | 38 (28.4) | < 0.001 |
| CAPO* | 77 (65.8) | 54 (40.3) | < 0.001 |
Data are given as mean ± SD or n (%).
Composite adverse perinatal outcome (CAPO) was defined as occurrence of at least one of the following: neonatal hypoglycemia, need for phototherapy, neonatal sepsis, respiratory distress syndrome, need for continuous positive airway pressure (CPAP), need for mechanical ventilation, 5‐min Apgar score < 7 or admission to neonatal intensive care unit (NICU). BMI, body mass index; GA, gestational age.
Doppler and biometric parameters
The mean ± SD gestational age at ultrasound examination was 30.04 ± 1.25 weeks in the early‐onset FGR group and 35.90 ± 1.14 weeks in the late‐onset FGR group (P < 0.001) (Table 3). UA‐PI values were significantly higher in early‐onset FGR at the right free loop and at the placental insertion site bilaterally, with borderline significance at the left free loop. EDF0 was observed more frequently at the placental insertion on both sides in early‐onset cases. EDF− was present only in early‐onset cases, most notably at the perivesical region.
Table 3.
Doppler and biometric parameters in 251 pregnancies with early‐ or late‐onset fetal growth restriction (FGR)
| Characteristic | Early‐onset FGR (n = 117) | Late‐onset FGR (n = 134) | P |
|---|---|---|---|
| GA at ultrasound (weeks) | 30.04 ± 1.25 | 35.90 ± 1.14 | < 0.001 |
| AC percentile | 1.58 ± 0.91 | 1.65 ± 0.89 | 0.560 |
| EFW percentile | 5.3 ± 2.9 | 5.3 ± 2.8 | 0.104 |
| Paravesical segment | |||
| Right UA‐PI | 1.18 ± 0.15 | 1.12 ± 0.17 | 0.225 |
| Right UA‐PI percentile | 84.5 ± 16.9 | 86.4 ± 11.9 | 0.191 |
| Right UA‐EDF0 | 39 (33.3) | 32 (23.9) | 0.113 |
| Right UA‐EDF− | 3 (2.6) | 0 (0) | 0.100 |
| Left UA‐PI | 1.14 ± 0.14 | 1.10 ± 0.15 | 0.131 |
| Left UA‐PI percentile | 79.0 ± 19.9 | 83.4 ± 13.3 | 0.143 |
| Left UA‐EDF0 | 30 (25.6) | 33 (24.6) | 0.880 |
| Left UA‐EDF− | 5 (4.3) | 0 (0) | 0.021 |
| Free loop | |||
| Right UA‐PI | 1.10 ± 0.17 | 1.01 ± 0.16 | 0.035 |
| Right UA‐PI percentile | 73.3 ± 23.1 | 75.1 ± 18.4 | 0.283 |
| Right UA‐EDF0 | 26 (22.2) | 18 (13.4) | 0.097 |
| Right UA‐EDF− | 2 (1.7) | 0 (0) | 0.216 |
| Left UA‐PI | 1.06 ± 0.16 | 1.00 ± 0.15 | 0.050 |
| Left UA‐PI percentile | 67.1 ± 21.1 | 73.2 ± 17.3 | 0.041 |
| Left UA‐EDF0 | 19 (16.2) | 17 (12.7) | 0.551 |
| Left UA‐EDF− | 1 (0.9) | 0 (0) | 0.466 |
| Placental insertion | |||
| Right UA‐PI | 1.06 ± 0.19 | 0.96 ± 0.17 | 0.015 |
| Right UA‐PI percentile | 65.3 ± 22.1 | 66.4 ± 19.3 | 0.213 |
| Right UA‐EDF0 | 15 (12.8) | 6 (4.5) | 0.033 |
| Right UA‐EDF− | 0 (0) | 0 (0) | NA |
| Left UA‐PI | 1.05 ± 0.20 | 0.95 ± 0.19 | 0.021 |
| Left UA‐PI percentile | 65.9 ± 21.5 | 66.0 ± 17.3 | 0.287 |
| Left UA‐EDF0 | 14 (12.0) | 4 (3.0) | 0.007 |
| Left UA‐EDF− | 0 (0) | 0 (0) | NA |
| MCA‐PI | 1.64 ± 0.27 | 1.48 ± 0.29 | 0.003 |
| MCA‐PSV | 38.1 ± 8.2 | 42.0 ± 5.9 | < 0.001 |
| Absent or reversed a‐wave in DV | 8 (6.8) | 1 (0.7) | 0.013 |
| CPR < 5th percentile | 32 (27.4) | 26 (19.4) | 0.176 |
Data are given as mean ± SD or n (%). AC, abdominal circumference; CPR, cerebroplacental ratio; DV, ductus venosus; EDF0, absent end‐diastolic flow; EDF−, reversed end‐diastolic flow; EFW, estimated fetal weight; GA, gestational age; MCA, middle cerebral artery; NA, not applicable; PI, pulsatility index; PSV, peak systolic velocity; UA, umbilical artery.
UA Doppler scores ranged from 0 to 18. For descriptive analyses, scores were categorized as 0–2, 3–5, 6–8, 9–12 and > 12 points. A score of 0–2 points was the most common score for both early‐ and late‐onset FGR, but was significantly less frequent in early‐onset FGR (87/117 (74.4%) vs 113/134 (84.3%); P = 0.049) (Table S1). In contrast, higher scores were more prevalent among early‐onset FGR cases (9–12 points: 13/117 (11.1%) vs 6/134 (4.5%); P = 0.047), suggesting more severe hemodynamic compromise.
Subgroup analysis stratified by UA Doppler score (< 3 vs ≥ 3 points) demonstrated a strong association between higher scores and adverse perinatal outcome in both FGR groups (Table 4). In early‐onset FGR, fetuses with an UA Doppler score ≥ 3 points delivered significantly earlier, had lower birth weights and showed markedly higher rates of NICU admission. Neonatal morbidities, including need for phototherapy, sepsis, RDS, need for CPAP, need for mechanical ventilation, 5‐min Apgar score < 7 and CAPO, were also significantly more frequent in early‐onset cases with UA Doppler score ≥ 3 points. In late‐onset FGR, UA Doppler score ≥ 3 points was associated with increased rates of NICU admission, need for phototherapy, RDS, 5‐min Apgar score < 7 and CAPO.
Table 4.
Obstetric and neonatal outcomes in early‐ and late‐onset fetal growth restriction (FGR), according to umbilical artery (UA) Doppler score
| Early‐onset FGR | Late‐onset FGR | |||||
|---|---|---|---|---|---|---|
| Outcome | UA score < 3 (n = 87) | UA score ≥ 3 (n = 30) | P | UA score < 3 (n = 113) | UA score ≥ 3 (n = 21) | P |
| GA at delivery (weeks) | 35.3 ± 2.4 | 31.4 ± 3.6 | < 0.001 | 37.0 ± 1.1 | 36.3 ± 1.0 | 0.007 |
| Preterm birth (< 37 weeks) | 38 (43.6) | 30 (100) | < 0.001 | 26 (23.0) | 15 (71.4) | < 0.001 |
| Mode of delivery | < 0.001 | 0.301 | ||||
| Vaginal | 69 (79.3) | 9 (30.0) | 97 (85.8) | 15 (71.4) | ||
| Cesarean section | 18 (20.7) | 21 (70.0) | 16 (14.2) | 6 (28.6) | ||
| Birth weight (g) | 2124 ± 318 | 1375 ± 562 | < 0.001 | 2305 ± 248 | 2242 ± 463 | 0.371 |
| Fetal distress leading to delivery | 12 (13.8) | 13 (43.3) | 0.002 | 24 (21.2) | 10 (47.6) | 0.023 |
| Corticosteroid treatment | 33 (37.9) | 24 (80.0) | < 0.001 | 10 (8.8) | 2 (9.5) | 0.921 |
| Intrauterine fetal demise | 0 (0) | 3 (10.0) | 0.016 | 0 (0) | 0 (0) | NA |
| Neonatal hypoglycemia | 26 (29.9) | 10 (33.3) | 0.902 | 12 (10.6) | 2 (9.5) | 0.879 |
| Phototherapy | 12 (13.8) | 12 (40.0) | 0.005 | 6 (5.3) | 4 (19.0) | 0.005 |
| Neonatal sepsis | 2 (2.3) | 5 (16.7) | 0.012 | 0 (0) | 0 (0) | NA |
| Transient tachypnea of the newborn | 39 (44.8) | 27 (90.0) | < 0.001 | 25 (22.1) | 19 (90.5) | < 0.001 |
| Respiratory distress syndrome | 25 (28.7) | 19 (63.3) | 0.002 | 9 (8.0) | 6 (28.6) | 0.018 |
| CPAP | 23 (26.4) | 23 (76.7) | < 0.001 | 11 (9.7) | 4 (19.0) | 0.254 |
| Mechanical ventilation | 17 (19.5) | 17 (56.7) | < 0.001 | 3 (2.7) | 0 (0) | > 0.999 |
| 5‐min Apgar score < 7 | 14 (16.1) | 13 (43.3) | < 0.001 | 4 (3.5) | 5 (23.8) | < 0.001 |
| NICU admission | 43 (49.4) | 30 (100) | < 0.001 | 27 (23.9) | 11 (52.4) | 0.017 |
| CAPO* | 47 (54.0) | 30 (100) | < 0.001 | 35 (31.0) | 19 (90.5) | < 0.001 |
Data are given as mean ± SD or n (%).
Composite adverse perinatal outcome (CAPO) was defined as occurrence of at least one of the following: neonatal hypoglycemia, need for phototherapy, neonatal sepsis, respiratory distress syndrome, need for continuous positive airway pressure (CPAP), need for mechanical ventilation, 5‐min Apgar score < 7 or admission to neonatal intensive care unit (NICU). GA, gestational age; NA, not applicable.
On multivariable logistic regression analysis adjusted for maternal age, BMI, parity, mode of conception, EFW percentile and gestational age at delivery, UA Doppler score analyzed as a continuous variable demonstrated an independent association with CAPO across models (Table 5). When analyzed as a dichotomous variable (≥ 3 points), UA Doppler score was associated with increased odds of CAPO (Model 1: aOR, 25.06 (95% CI, 4.31–145.48); Nagelkerke R 2 = 0.695; overall accuracy, 86.1%). Abnormal free‐loop UA Doppler was also associated independently with CAPO (Model 2: aOR, 8.57 (95% CI, 3.39–21.62); Nagelkerke R 2 = 0.705; overall accuracy, 87.6%). In the combined model including abnormal free‐loop UA Doppler and continuous UA Doppler score (Model 3), both variables were associated significantly with CAPO (aOR, 3.52 (95% CI, 1.21–10.24) and 2.02 (95% CI, 1.21–3.36), respectively). This model demonstrated the highest explanatory performance (Nagelkerke R 2 = 0.739; overall accuracy, 88.0%). In the model including abnormal free‐loop UA Doppler and dichotomized UA Doppler score (≥ 3 points) (Model 4), UA Doppler score was associated independently with CAPO (aOR, 9.74 (95% CI, 1.54–61.33)). Abnormal free‐loop UA Doppler was also associated with CAPO, although with a smaller effect size (aOR, 5.27 (95% CI, 1.94–14.25)). This combined model demonstrated good explanatory performance (Nagelkerke R 2 = 0.723), with an overall classification accuracy of 87.3%. When analyzed as a continuous variable alone (Model 5), UA Doppler score was associated independently with CAPO (aOR, 2.64 (95% CI, 1.59–4.39); Nagelkerke R 2 = 0.726; overall accuracy, 88.0%). In contrast, MCA‐PI was not associated significantly with CAPO (Model 6: aOR, 1.32 (95% CI, 0.42–4.08); Nagelkerke R 2 = 0.646; overall accuracy, 83.3%).
Table 5.
Multivariable logistic regression analysis of factors associated with composite adverse perinatal outcome in pregnancies with fetal growth restriction
| Model | B | SE | Wald | aOR (95% CI) | P |
|---|---|---|---|---|---|
| Model 1 | |||||
| Maternal age* | 0.003 | 0.04 | 0.65 | 1.03 (0.95–1.11) | 0.422 |
| BMI at presentation† | −0.03 | 0.05 | 0.32 | 0.97 (0.87–1.07) | 0.567 |
| Nulliparous | 0.89 | 0.51 | 3.14 | 2.44 (0.91–4.55) | 0.076 |
| Conception via IVF | −0.70 | 0.55 | 1.57 | 0.49 (0.16–1.48) | 0.209 |
| EFW percentile‡ | 0.01 | 0.01 | 0.39 | 1.00 (0.98–1.00) | 0.529 |
| GA at delivery§ | −2.21 | 0.35 | 38.80 | 0.11 (0.05–0.21) | < 0.001 |
| UA Doppler score ≥ 3 | 3.22 | 0.89 | 12.80 | 25.06 (4.31–145.48) | < 0.001 |
| Model 2 | |||||
| Maternal age* | 0.05 | 0.04 | 1.35 | 1.05 (0.96–1.14) | 0.245 |
| BMI at presentation† | −0.03 | 0.05 | 0.42 | 0.96 (0.86–1.07) | 0.513 |
| Nulliparous | 0.43 | 0.47 | 0.82 | 1.53 (0.61–3.88) | 0.363 |
| Conception via IVF | −0.37 | 0.58 | 0.39 | 0.69 (0.21–2.18) | 0.528 |
| EFW percentile‡ | 0.01 | 0.01 | 0.46 | 1.00 (0.99–1.00) | 0.493 |
| GA at delivery§ | −1.95 | 0.32 | 35.50 | 0.14 (0.07–0.26) | < 0.001 |
| Abnormal free‐loop UA Doppler | 2.14 | 0.47 | 20.70 | 8.57 (3.39–21.62) | < 0.001 |
| Model 3 | |||||
| Maternal age* | 0.05 | 0.04 | 1.41 | 1.05 (0.96–1.14) | 0.234 |
| BMI at presentation† | −0.03 | 0.06 | 0.36 | 0.96 (0.86–1.08) | 0.547 |
| Nulliparous | 0.71 | 0.51 | 1.88 | 2.01 (0.74–5.47) | 0.170 |
| Conception via IVF | −0.25 | 0.58 | 0.65 | 0.77 (0.24–2.42) | 0.417 |
| EFW percentile‡ | 0.01 | 0.01 | 0.22 | 1.00 (0.99–1.00) | 0.638 |
| GA at delivery§ | −2.01 | 0.35 | 32.1 | 0.13 (0.06–0.27) | < 0.001 |
| Abnormal free‐loop UA Doppler | 1.25 | 0.54 | 5.33 | 3.52 (1.21–10.24) | 0.021 |
| UA Doppler score¶ | 0.71 | 0.26 | 7.30 | 2.02 (1.21–3.36) | 0.007 |
| Model 4 | |||||
| Maternal age* | 0.05 | 0.04 | 1.35 | 1.05 (0.96–1.14) | 0.244 |
| BMI at presentation† | −0.04 | 0.05 | 0.52 | 0.95 (0.85–1.07) | 0.470 |
| Nulliparous | 0.87 | 0.52 | 2.79 | 2.41 (0.86–6.71) | 0.095 |
| Conception via IVF | −0.41 | 0.58 | 0.49 | 0.66 (0.21–2.07) | 0.481 |
| EFW percentile‡ | 0.01 | 0.01 | 0.06 | 1.00 (1.00–1.00) | 0.799 |
| GA at delivery§ | −2.00 | 0.34 | 34.57 | 0.13 (0.07–0.26) | < 0.001 |
| Abnormal free‐loop UA Doppler | 1.66 | 0.51 | 10.72 | 5.27 (1.94–14.25) | 0.001 |
| UA Doppler score ≥ 3 | 2.27 | 0.93 | 5.88 | 9.74 (1.54–61.33) | 0.015 |
| Model 5 | |||||
| Maternal age* | 0.04 | 0.04 | 0.92 | 1.04 (0.95–1.13) | 0.336 |
| BMI at presentation† | −0.03 | 0.06 | 0.28 | 0.97 (0.86–1.08) | 0.594 |
| Nulliparous | 0.68 | 0.50 | 1.85 | 1.97 (0.74–5.29) | 0.174 |
| Conception via IVF | −0.39 | 0.57 | 0.46 | 0.67 (0.22–2.07) | 0.494 |
| EFW percentile‡ | 0.01 | 0.01 | 0.07 | 1.00 (0.99–1.00) | 0.781 |
| GA at delivery§ | −2.17 | 0.36 | 35.12 | 0.11 (0.05–0.23) | < 0.001 |
| UA Doppler score¶ | 0.97 | 0.25 | 14.24 | 2.64 (1.59–4.39) | < 0.001 |
| Model 6 | |||||
| Maternal age* | 0.02 | 0.04 | 0.41 | 1.03 (0.95–1.11) | 0.518 |
| BMI at presentation† | −0.01 | 0.05 | 0.07 | 0.98 (0.89–1.09) | 0.791 |
| Nulliparous | 0.15 | 0.42 | 0.13 | 1.16 (0.51–2.67) | 0.713 |
| Conception via IVF | −0.77 | 0.56 | 1.94 | 0.46 (0.15–1.37) | 0.164 |
| EFW percentile‡ | 0.01 | 0.01 | 2.36 | 1.00 (1.00–1.00) | 0.124 |
| GA at delivery§ | −2.24 | 0.34 | 41.20 | 0.10 (0.05–0.21) | < 0.001 |
| MCA‐PI** | 0.27 | 0.57 | 0.23 | 1.32 (0.42–4.08) | 0.628 |
All models showed statistically significant overall fit (omnibus test, all P < 0.001). Nagelkerke R 2 values ranged from 0.646 to 0.739 and overall classification accuracy ranged from 83.3% to 88.0%. Abnormal free‐loop umbilical artery (UA) Doppler was defined as UA pulsatility index (PI) ≥ 95th percentile and/or absent or reversed end‐diastolic flow.
Per 1‐year increase.
Per 1‐kg/m2 increase.
Per 1‐percentile increase.
Per 1‐week increase.
Per 1‐point increase.
Per 1‐unit increase. aOR, adjusted odds ratio; BMI, body mass index; EFW, estimated fetal weight; GA, gestational age; IVF, in‐vitro fertilization; MCA, middle cerebral artery; SE, standard error.
The rate of CAPO increased progressively with rising UA Doppler score, demonstrating a significant linear trend across categories (P < 0.001) (Table S2). CAPO was present in 41.0% of fetuses with an UA Doppler score of 0–2 points, whereas all fetuses with an UA Doppler score ≥ 6 points experienced CAPO. When markers of fetoplacental hemodynamic deterioration were examined separately, abnormal DV Doppler, CPR < 5th percentile, fetal distress leading to delivery and 5‐min Apgar score < 7 showed significant linear trends across increasing UA Doppler score categories in both early‐ and late‐onset FGR (Table 6). The rate of intrauterine fetal demise also rose across increasing UA Doppler score categories in early‐onset FGR, although no events occurred in the late‐onset group.
Table 6.
Prevalence of markers of fetoplacental hemodynamic deterioration according to umbilical artery (UA) Doppler score, stratified by early‐ or late‐onset fetal growth restriction (FGR)
| UA Doppler score | Absent or reversed a‐wave in DV | CPR < 5th percentile | Intrauterine fetal demise | Fetal distress leading to delivery | 5‐min Apgar score < 7 |
|---|---|---|---|---|---|
| Early‐onset FGR | |||||
| 0–2 points (n = 87) | 0 (0) | 16 (18.4) | 0 (0) | 12 (13.8) | 14 (16.1) |
| 3–5 points (n = 7) | 1 (14.3) | 3 (42.9) | 0 (0) | 2 (28.6) | 3 (42.9) |
| 6–8 points (n = 8) | 1 (12.5) | 4 (50.0) | 1 (12.5) | 3 (37.5) | 3 (37.5) |
| 9–12 points (n = 13) | 4 (30.8) | 7 (53.8) | 1 (7.7) | 6 (46.2) | 5 (38.5) |
| > 12 points (n = 2) | 2 (100) | 2 (100) | 1 (50.0) | 2 (100) | 2 (100) |
| P for trend | < 0.001 | < 0.001 | 0.018 | < 0.001 | < 0.001 |
| Late‐onset FGR | |||||
| 0–2 points (n = 113) | 0 (0) | 19 (16.8) | 0 (0) | 24 (21.2) | 4 (3.5) |
| 3–5 points (n = 9) | 0 (0) | 2 (22.2) | 0 (0) | 3 (33.3) | 1 (11.1) |
| 6–8 points (n = 6) | 0 (0) | 2 (33.3) | 0 (0) | 3 (50.0) | 1 (16.7) |
| 9–12 points (n = 6) | 1 (16.7) | 3 (50.0) | 0 (0) | 5 (83.3) | 3 (50.0) |
| > 12 points (n = 0) | NA | NA | NA | NA | NA |
| P for trend | 0.018 | 0.021 | — | < 0.001 | 0.002 |
Data are given as n (%). Linear trend across increasing UA Doppler score categories was evaluated using Cochran–Armitage test for trend. CPR, cerebroplacental ratio; DV, ductus venosus; NA, not applicable.
Discussion
In this study, we evaluated UA Doppler flow across multiple cord segments in singleton pregnancies complicated by FGR. Using a novel segment‐based Doppler scoring system ranging from 0 to 18 and derived from EDF abnormalities at six predefined anatomical sites, we demonstrated a clear and graded association between higher UA Doppler score and adverse perinatal outcome. These findings support the potential clinical value of this scoring system as a tool for risk stratification in both early‐ and late‐onset FGR. Although previous studies have demonstrated the prognostic value of abnormal UA Doppler in FGR, to our knowledge, this is the first prospective study to systematically apply and clinically validate a standardized, multisite UA Doppler scoring approach in both early‐ and late‐onset FGR populations.
UA Doppler velocimetry is a cornerstone of FGR surveillance, as it directly reflects fetoplacental vascular resistance and serves as an indirect marker of placental function 19 . Current clinical guidelines emphasize that abnormal UA Doppler findings are among the earliest detectable signs of placental dysfunction in FGR and typically appear several weeks before significant clinical abnormalities are observed 1 , 19 . The clinical efficacy of UA Doppler in the surveillance of high‐risk pregnancies was demonstrated in the Cochrane systematic review of Alfirevic et al., which reported a significant reduction in perinatal mortality, along with lower rates of labor induction and Cesarean delivery, in high‐risk pregnancies monitored using UA Doppler, thereby reinforcing its fundamental role in the management of FGR 10 . Although UA Doppler velocimetry has been in use for decades and is endorsed by international guidelines, the methodological approach for UA Doppler assessment has remained fundamentally unchanged since it was first defined 20 , 21 . The currently accepted protocol is based on a single UA measurement taken from the middle portion of the umbilical cord. This conventional approach presumes relative hemodynamic homogeneity both longitudinally along the umbilical cord and between the paired UAs 22 . However, the presence of two anatomically distinct UAs is well established, and experimental as well as clinical studies have long demonstrated that vascular resistance varies along the cord, with higher impedance at the perivesical segments and lower impedance toward the placental insertion 23 , 24 .
Hyrtl's anastomosis forms an interarterial connection near the placental insertion and may influence distal flow distribution between the two UAs 25 . However, its presence, caliber and functional patency are variable, and complete hemodynamic homogenization cannot be assumed. Because this interarterial connection can modulate distal resistance, segmental PI or EDF abnormalities at the placental insertion may not always represent independent hemodynamic deterioration, and the possibility of misclassification should therefore be considered. The long‐held assumption that Hyrtl's anastomosis uniformly equalizes flow between the two UAs has been increasingly challenged. While this anastomosis may partially balance distal resistance, accumulating evidence indicates that clinically meaningful differences can exist not only between cord segments but also between the left and right UAs 22 . Supporting this concept, Steller et al. reported discordant UA Doppler findings in 16.7% of 425 fetuses with FGR, with one artery exhibiting an abnormal PI while the contralateral artery remained within normal PI limits 14 .
Therefore, the number of arteries sampled and the anatomical site of measurement may influence significantly the clinical interpretation and subsequent treatment decisions. Park et al. demonstrated that, in 40.8% of fetuses with EDF0 or EDF− detected in the free‐floating cord, Doppler waveforms differed between the left and right UAs at the intra‐abdominal perivesical level 26 . These findings underscore that preserved forward flow in one artery does not necessarily exclude significant pathological resistance in the other. Despite these observations, existing national and international guidelines do not address whether both UAs should be assessed routinely or how sampling site selection may influence clinical decision‐making 15 , 27 , 28 , 29 .
The scoring system proposed in this study was inspired conceptually by Paladini's recent call for a more anatomically informed and structured approach to UA Doppler assessment in FGR 18 . While that proposal introduced a four‐site system and a 10‐point scoring scale based on the presence and direction of EDF patterns, our study expands this concept by incorporating six anatomical locations (bilateral perivesical, free‐loop and placental insertion sites in each UA), resulting in a broader scoring range of 0–18. This expanded design aimed to capture more comprehensively the extent and distribution of fetoplacental vascular resistance. The rationale was that subtle or segmentally confined Doppler abnormalities, especially when unilateral or confined to a single site, might be overlooked by conventional mid‐cord single‐vessel sampling.
By quantifying EDF abnormalities across multiple regions, the scoring system provided a structured representation of spatial Doppler heterogeneity and demonstrated significant associations with perinatal outcome within this cohort. This anatomically expanded approach offers a more comprehensive characterization of UA flow distribution compared with conventional single‐site assessment.
The principal strengths of this study lie in its prospective design and inclusion of a well‐characterized cohort of both early‐ and late‐onset FGR cases managed using a standardized clinical protocol. However, several limitations should be acknowledged. First, although Doppler evaluations were performed systematically across six anatomical sites, technical challenges in obtaining reliable waveforms, particularly at the placental and perivesical insertions, may limit reproducibility and make acquisition of technically adequate UA Doppler signals more difficult in routine clinical practice, especially in advanced gestational ages. Second, while our scoring system integrates segmental and bilateral Doppler data, we did not include direct correlation with postnatal placental histopathology, which could have enhanced pathophysiological interpretation. The use of CAPO as an unweighted composite outcome represents an additional limitation. Its individual components are heterogeneous in clinical severity and prognostic relevance. Moreover, several elements may be influenced by local neonatal practice patterns and institutional thresholds for NICU admission, potentially limiting the precision with which the overall burden of adverse outcome is captured. Finally, although this study demonstrates a strong cross‐sectional association between the proposed score and perinatal outcome, future prospective studies with serial assessments and interventional designs are required to determine whether evaluating dynamic longitudinal changes in UA Doppler score may improve clinical decision‐making and neonatal outcome.
In conclusion, this study describes a novel segment‐based UA Doppler scoring system for the assessment of FGR and demonstrates a strong and independent association between higher scores and adverse perinatal outcome in both early‐onset and late‐onset FGR cases within our cohort. The findings suggest that evaluating UA flow across multiple anatomical sites provides a broader characterization of Doppler patterns compared with conventional single‐site assessment. Further prospective intervention‐based studies are needed to evaluate the clinical benefit and feasibility of integrating this scoring system into routine obstetric practice.
Supporting information
Appendix S1 Calculator for predicted probability of composite adverse perinatal outcome in pregnancy with fetal growth restriction, based on multisite bilateral umbilical artery Doppler assessment.
Table S1 Distribution of umbilical artery Doppler scores in early‐ vs late‐onset fetal growth restriction.
Table S2 Rates of composite adverse perinatal outcome according to umbilical artery Doppler score.
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
- 1. Lees CC, Stampalija T, Baschat A, et al. ISUOG Practice Guidelines: diagnosis and management of small‐for‐gestational‐age fetus and fetal growth restriction. Ultrasound Obstet Gynecol. 2020;56(2):298‐312. [DOI] [PubMed] [Google Scholar]
- 2. Piergianni M, Della Valle L, Khalil A, et al. Perinatal and maternal outcomes of extremely early‐onset fetal growth restriction (≤ 26 weeks): systematic review and meta‐analysis. Ultrasound Obstet Gynecol. 2026;67(4):444‐454. [DOI] [PubMed] [Google Scholar]
- 3. Pels A, Beune IM, van Wassenaer‐Leemhuis AG, Limpens J, Ganzevoort W. Early‐onset fetal growth restriction: a systematic review on mortality and morbidity. Acta Obstet Gynecol Scand. 2020;99(2):153‐166. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4. McCowan LM, Figueras F, Anderson NH. Evidence‐based national guidelines for the management of suspected fetal growth restriction: comparison, consensus, and controversy. Am J Obstet Gynecol. 2018;218(2S):S855‐S868. [DOI] [PubMed] [Google Scholar]
- 5. Molina LCG, Odibo L, Zientara S, et al. Validation of Delphi procedure consensus criteria for defining fetal growth restriction. Ultrasound Obstet Gynecol. 2020;56(1):61‐66. [DOI] [PubMed] [Google Scholar]
- 6. Gordijn SJ, Beune IM, Thilaganathan B, et al. Consensus definition of fetal growth restriction: a Delphi procedure. Ultrasound Obstet Gynecol. 2016;48(3):333‐339. [DOI] [PubMed] [Google Scholar]
- 7. Figueras F, Gratacos E. An integrated approach to fetal growth restriction. Best Pract Res Clin Obstet Gynaecol. 2017;38:48‐58. [DOI] [PubMed] [Google Scholar]
- 8. Sacchi C, Marino C, Nosarti C, Vieno A, Visentin S, Simonelli A. Association of intrauterine growth restriction and small for gestational age status with childhood cognitive outcomes: a systematic review and meta‐analysis. JAMA Pediatr. 2020;174(8):772‐781. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Lees CC, Marlow N, van Wassenaer‐Leemhuis A, et al. 2 year neurodevelopmental and intermediate perinatal outcomes in infants with very preterm fetal growth restriction (TRUFFLE): a randomised trial. Lancet. 2015;385(9983):2162‐2172. [DOI] [PubMed] [Google Scholar]
- 10. Alfirevic Z, Stampalija T, Dowswell T. Fetal and umbilical Doppler ultrasound in high‐risk pregnancies. Cochrane Database Syst Rev. 2017;6(6):CD007529. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. Lees CC, Romero R, Stampalija T, et al. Clinical opinion: the diagnosis and management of suspected fetal growth restriction: an evidence‐based approach. Am J Obstet Gynecol. 2022;226(3):366‐378. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Bhide A, Acharya G, Baschat A, et al. ISUOG Practice Guidelines (updated): use of Doppler velocimetry in obstetrics. Ultrasound Obstet Gynecol. 2021;58(2):331‐339. [DOI] [PubMed] [Google Scholar]
- 13. Acharya G, Wilsgaard T, Berntsen GKR, 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(2):162‐169. [DOI] [PubMed] [Google Scholar]
- 14. Steller JG, Driver C, Gumina D, et al. Doppler velocimetry discordance between paired umbilical artery vessels and clinical implications in fetal growth restriction. Am J Obstet Gynecol. 2022;227(2):285.e1‐285.e7. [DOI] [PubMed] [Google Scholar]
- 15. Martins JG, Biggio JR, Abuhamad A. Society for Maternal‐Fetal Medicine Consult Series #52: diagnosis and management of fetal growth restriction: (Replaces Clinical Guideline Number 3, April 2012). Am J Obstet Gynecol. 2020;223(4):B2‐B17. [DOI] [PubMed] [Google Scholar]
- 16. Drukker L, Staines‐Urias E, Villar J, et al. International gestational age‐specific centiles for umbilical artery Doppler indices: a longitudinal prospective cohort study of the INTERGROWTH‐21st Project. Am J Obstet Gynecol. 2020;222(6):602.e1‐602.e15. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17. Acharya G, Wilsgaard T, Berntsen GKR, Maltau JM, Kiserud T. Reference ranges for serial measurements of umbilical artery Doppler indices in the second half of pregnancy. Am J Obstet Gynecol. 2005;192(3):937‐944. [DOI] [PubMed] [Google Scholar]
- 18. Paladini D. Umbilical artery Doppler: is all said and done? Ultrasound Obstet Gynecol. 2025;65(2):137‐141. [DOI] [PubMed] [Google Scholar]
- 19. Fetal Growth Restriction . ACOG Practice Bulletin, Number 227. Obstet Gynecol. 2021;137(2):e16‐e28. [DOI] [PubMed] [Google Scholar]
- 20. FitzGerald DE, Drumm JE. Non‐invasive measurement of human fetal circulation using ultrasound: a new method. Br Med J. 1977;2(6100):1450‐1451. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21. Pearce JM, Campbell S. Intrauterine growth retardation. Birth Defects Orig Artic Ser. 1985;21(5):109‐130. [PubMed] [Google Scholar]
- 22. Ullberg U, Sandstedt B, Lingman G. Hyrtl's anastomosis, the only connection between the two umbilical arteries. A study in full term placentas from AGA infants with normal umbilical artery blood flow. Acta Obstet Gynecol Scand. 2001;80(1):1‐6. [DOI] [PubMed] [Google Scholar]
- 23. Khare M, Paul S, Konje JC. Variation in Doppler indices along the length of the cord from the intraabdominal to the placental insertion. Acta Obstet Gynecol Scand. 2006;85(8):922‐928. [DOI] [PubMed] [Google Scholar]
- 24. Janeczek S, MacMillan W, Besinger R, Weisenborn E, Mittendorf R. Left versus right intra‐abdominal umbilical arteries: a comparison of their doppler waveforms. Am J Obstet Gynecol. 2003;189(6):S185. [Google Scholar]
- 25. Mangla M, Motwani R, Palo S. Anatomical and functional insights into Hyrtl's anastomosis: implications for placental and fetal vascular dynamics. Clin Anat. 2025. doi:10.1002/ca.70027 [DOI] [PubMed] [Google Scholar]
- 26. Park JW, Lee SM, Kang HS, Shim SS, Jun JK. Discrepancy in Doppler waveforms between two umbilical arteries in fetuses with absent or reversed end‐diastolic flow: a prospective observational study. J Clin Ultrasound. 2019;47(9):526‐530. [DOI] [PubMed] [Google Scholar]
- 27. Aprile A, Calì G, Chianchiano N, et al. Corrigendum to “The Italian guidelines on ultrasound in obstetrics and gynecology: Executive summary of recommendations for practice” [Eur. J. Obstetrics Gynecol. 279 (2022) 176‐182]. Eur J Obstet Gynecol Reprod Biol. 2023;281:85‐86. [DOI] [PubMed] [Google Scholar]
- 28. Vayssière C, Sentilhes L, Ego A, et al. Fetal growth restriction and intra‐uterine growth restriction: guidelines for clinical practice from the French College of Gynaecologists and Obstetricians. Eur J Obstet Gynecol Reprod Biol. 2015;193:10‐18. [DOI] [PubMed] [Google Scholar]
- 29. Kingdom J, Ashwal E, Lausman A, et al. Guideline No 442: fetal growth restriction: screening, diagnosis, and management in singleton pregnancies. J Obstet Gynaecol Can. 2023;45(10):102154. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Appendix S1 Calculator for predicted probability of composite adverse perinatal outcome in pregnancy with fetal growth restriction, based on multisite bilateral umbilical artery Doppler assessment.
Table S1 Distribution of umbilical artery Doppler scores in early‐ vs late‐onset fetal growth restriction.
Table S2 Rates of composite adverse perinatal outcome according to umbilical artery Doppler score.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.