Fetal phenotypes at a late third trimester scan: classification of risk and contribution to adverse outcomes

Fetal phenotypes at a late third trimester scan: classification of risk and contribution to adverse outcomes | Authorea try { document.documentElement.classList.add('js'); } catch (e) { } var _gaq = _gaq || []; _gaq.push(['_setAccount', 'G-8VDV14Y67G']); _gaq.push(['_trackPageview']); (function() { var ga = document.createElement('script'); ga.type = 'text/javascript'; ga.async = true; ga.src = ('https:' == document.location.protocol ? 'https://ssl' : 'http://www') + '.google-analytics.com/ga.js'; var s = document.getElementsByTagName('script')[0]; s.parentNode.insertBefore(ga, s); })(); Skip to main content Preprints Collections Wiley Open Research IET Open Research Ecological Society of Japan All Collections About About Authorea FAQs Contact Us Quick Search anywhere Search for preprint articles, keywords, etc. Search Search ADVANCED SEARCH SCROLL BJOG: An International Journal of Obstetrics and Gynaecology This is a preprint and has not been peer reviewed. Data may be preliminary. 3 September 2025 V1 Latest version Share on Fetal phenotypes at a late third trimester scan: classification of risk and contribution to adverse outcomes Authors : Elena D’Alberti 0000-0003-0526-6329 , Chiara Granieri , Christos Ioannou , Christina Y.L. Aye , Michael Shea , and Lawrence Impey 0000-0002-4462-112X [email protected] Authors Info & Affiliations https://doi.org/10.22541/au.175689562.29509572/v1 245 views 145 downloads Contents Abstract Supplementary Material Information & Authors Metrics & Citations View Options References Figures Tables Media Share Abstract ABSTRACT Objective To examine the contribution of different ultrasonographic fetal growth phenotypes to adverse perinatal outcomes at term. Design Retrospective population-based cohort study. Setting John Radcliffe Hospital, Oxford, where universal ultrasound at 35 +1 -36 +6 weeks is performed. Population Congenital abnormalities and births before the scan were excluded. Singleton fetuses were categorized as five mutually exclusive phenotypes using a hierarchical approach: 1. ISUOG fetal growth restriction (FGR), according to Delphi criteria; 2. Constitutional small-for-gestational-age (SGA) (estimated fetal weight [EFW] <10 th centile); 3. Appropriate-for-gestational-age (AGA) with either cerebroplacental ratio 95 th centile; 4. AGA with slowing abdominal circumference growth velocity (ACGV <10 th centile); 5. Normal AGA; Methods Univariate logistic regression was employed using normal AGA as reference group. Group differences were assessed using the chi-square test and ANOVA. Main outcome measures Stillbirth (SB); composite adverse outcome (CAO) (1+ of Grade 2-3 encephalopathy, cooling, ventilation >24 hours, or perinatal death); severe SGA at birth; neonatal unit admission; obstetric interventions. Results Among 45179 pregnancies, 54 SBs (0.1%) and 253 CAOs (0.6%) occurred. Normal AGA fetuses at the 35 +1 -36 +6 week scan accounted for 82% of all pregnancies and for 43 (79.6%) SBs and 205 (81%) with the CAO, yet only 37.3% of neonates born with severe SGA. The absolute risk of SB and CAO was similar in all groups (0.1-0.2%), with the highest intervention rates in Group 1. Conclusions Term FGR and ‘normal’ babies have similar perinatal risks, presumably because of intervention. Despite a detection rate of 62.7% for severe SGA, most adverse outcomes occurred in pregnancies with a normal scan. Funding Oxford Hospitals Charity. Registered charity number 1175809 Fetal phenotypes at a late third trimester scan: classification of risk and contribution to adverse outcomes Elena D’Alberti, 1,2 Chiara Granieri 1,3 , Christos Ioannou 1,4 , Christina Y. Aye 1,4 , Michael Shea 4 , Lawrence Impey 1,4 1 Nuffield Department of Women’s & Reproductive Health, University of Oxford, University of Oxford, Oxford, UK, Headington, OX3 9DU 2 Department of Maternal and Child Health and Urological Sciences, Sapienza University of Rome, Rome, Italy, Viale del Policlinico 155 3 Department of Obstetrics and Gynecology, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy, Largo A. Gemelli, 8 4 Women’s Centre, John Radcliffe Hospital, Oxford University Hospitals NHS Foundation Trust, Oxford, UK, Headington, OX3 9DU Short title: Burden of perinatal risk and late third trimester scan findings Corresponding author: Lawrence Impey Women’s Centre, John Radcliffe Hospital Oxford University Hospitals NHS Foundation Trust, Oxford, UK email: [email protected] Objective To examine the contribution of different ultrasonographic fetal growth phenotypes to adverse perinatal outcomes at term. Design Retrospective population-based cohort study. Setting John Radcliffe Hospital, Oxford, where universal ultrasound at 35 +1 -36 +6 weeks is performed. Population Congenital abnormalities and births before the scan were excluded. Singleton fetuses were categorized as five mutually exclusive phenotypes using a hierarchical approach: 1. ISUOG fetal growth restriction (FGR), according to Delphi criteria; 2. Constitutional small-for-gestational-age (SGA) (estimated fetal weight [EFW] <10 th centile); 3. Appropriate-for-gestational-age (AGA) with either cerebroplacental ratio 95 th centile; 4. AGA with slowing abdominal circumference growth velocity (ACGV 5. Normal AGA; Methods Univariate logistic regression was employed using normal AGA as reference group. Group differences were assessed using the chi-square test and ANOVA. Main outcome measures Stillbirth (SB); composite adverse outcome (CAO) (1+ of Grade 2-3 encephalopathy, cooling, ventilation >24 hours, or perinatal death); severe SGA at birth; neonatal unit admission; obstetric interventions. Results Among 45179 pregnancies, 54 SBs (0.1%) and 253 CAOs (0.6%) occurred. Normal AGA fetuses at the 35 +1 -36 +6 week scan accounted for 82% of all pregnancies and for 43 (79.6%) SBs and 205 (81%) with the CAO, yet only 37.3% of neonates born with severe SGA. The absolute risk of SB and CAO was similar in all groups (0.1-0.2%), with the highest intervention rates in Group 1. Conclusions Term FGR and ‘normal’ babies have similar perinatal risks, presumably because of intervention. Despite a detection rate of 62.7% for severe SGA, most adverse outcomes occurred in pregnancies with a normal scan. Funding Oxford Hospitals Charity. Registered charity number 1175809 K E Y W O R D S: universal scan; third trimester; stillbirth; adverse perinatal outcomes; small-for-gestational-age (SGA); fetal growth restriction (FGR); FUNDING This study was supported by the Oxford Hospitals Charity (registered charity number 1175809). The funder of this study had no role in study design, data collection, analysis or interpretation of the data, in writing the paper or the decision to submit for publication. INTRODUCTION Identification of fetuses at higher risk of adverse perinatal outcomes is the cornerstone of obstetric care. Established risk factors for increased perinatal morbidity and mortality include small for gestational age (SGA), when biometry falls below the 10 th centile according to a population-based reference, and fetal growth restriction (FGR), a more complex condition, defined by the Delphi criteria, and characterized by multiple aetiologies. 1 Significant efforts in many healthcare systems, such as the implementation of care pathways to identify FGR, or even a universal third-trimester ultrasound, have aimed to improve the identification of affected pregnancies. 2-4 In fetuses prenatally identified as SGA or FGR, reduced rates of stillbirth have been reported. 5 Nevertheless, the association at least between SGA and perinatal death is much weaker at term than it is preterm, with only 30% of term stillbirths reported as SGA in a recent nationwide cohort study, 6 with an unknown but presumed higher proportion of babies with FGR. This has driven the search for alternative ultrasonographic markers, such as cerebroplacental ratio (CPR) 7 or fetal growth velocity (FGV), 8 to identify a wider spectrum of placental dysfunction, and enable a better risk stratification of appropriate-for-gestational age (AGA) fetuses. It remains unclear, however, how many term stillbirths have identifiable FGR and what level of risk is associated with different classifications of FGR. The aim of this study was to determine the rate of adverse outcomes according to FGR phenotype at a universally performed ultrasound at 35 +1 to 36 +6 weeks and assess the contribution of antenatally diagnosed FGR to adverse outcomes at or near term. METHODS Study design and setting This was a retrospective population-based cohort study from Oxford, UK of singleton pregnancies, dated by crown-rump length (CRL), with an estimated due date between 01/10/2016 and 31/12/2023, undergoing a ‘universal’ scan between 35 +1 and 36 +6 weeks. Exclusion criteria were multiple pregnancies, those with congenital abnormalities diagnosed prenatally, those who gave birth before the scan, or did not have it, and those with missing perinatal outcome data (Figure 1). In this unit all singleton pregnancies are offered a universal routine scan between 35 +1 and 36 +6 weeks, irrespective of prior risk, with earlier additional scans performed according to risk stratification based on universal uterine artery Doppler at 18-21 weeks, and established clinical maternal risk factors. At the routine scan, the estimated fetal weight (EFW), crude growth velocity since 20 weeks, fetal Doppler velocimetry of the umbilical artery (UAPI), middle cerebral artery (MCA PI) and cerebroplacental ratio (CPR) are measured according to ISUOG Guidelines, 9,10 using quality assurance methodology. 11 Fetuses with an EFW 95 th centile 13 or abnormal CPR (< 1.1) were managed according to a published protocol. 14 The impact of the universal 36 week scan on adverse outcomes has been previously described. 14 Fetal growth phenotypes were sequentially categorized into five mutually exclusive groups based on established criteria for SGA and FGR patterns, according to the EFW, growth velocity, CPR and UAPI: ISUOG FGR , defined according to the Delphi criteria, with either an EFW < 3 rd centile or the combination of at least 2 of the following criteria: EFW < 10 th centile, 12 CPR 95 th centile, 13 or AC/EFW crossing more than 2 quartiles; 1 SGA , with an EFW < 10 th centile, but not meeting criteria for Group 1. 1 The remaining AGA babies were sequentially categorized as: 1. AGA with abnormal Dopplers , defined as an EFW ≥ 10 th centile 12 associated with either the CPR 95 th centile. 13 This group was chosen as previous studies have shown these pregnancies to be at higher risk of adverse outcomes. 7 2. AGA with abdominal circumference growth velocity (ACGV) < 10 th centile , defined by an EFW ≥ 10 th centile 12 with a deceleration in the AC growth, from mid-trimester to the routine scan, <10 th centile. This group was chosen as a low ACGV has been previously shown to be a significant risk factor for composite adverse outcomes, at least among SGA fetuses. 15,16 3. Normal AGA , defined as the presence of an EFW ≥ 10 th centile 12 with neither an ACGV ≥ 10 th centile nor abnormal Doppler indices. This study was approved by the Health Research Authority (IRAS project ID: 222260; REC reference: 17/SC/0374, updated July 2024). The study was reported according to the STROBE reporting standards and guidelines. Outcomes The primary outcome was stillbirth. The secondary outcomes were a) a composite of severe adverse outcomes (CAO), defined as at least one of stillbirth or neonatal death 24 hours; b) severe SGA with a birthweight < 3 rd centile; 17 and c) neonatal unit (NNU) admission and d) intervention rates including caesarean section (CS) and induction of labour. Data sources Routinely-collected pregnancy clinical/demographic data were extracted from Cerner Millennium (London, UK) and neonatal data was extracted from BadgerNet (Clevermed, Edinburgh, UK). Ultrasound data was extracted from ViewPoint 5 (GE Healthcare, Chicago, IL, USA). Analysis Scan findings were categorized for the mutually exclusive groups, and maternal and neonatal characteristics were summarized in each group. Continuous variables were presented as mean ± standard deviation (SD) or median with interquartile range (IQR), and categorical variables as proportions (n %). Missing covariate data were excluded when < 5%. A generalized linear model with binary logistic function was employed for univariate logistic regression to evaluate the associations between growth phenotypes and binary outcomes. Multi-categorical comparisons used dummy coding, with the constitutional AGA group as the reference category. Results were expressed as odds ratios (ORs) with 95% confidence intervals (CIs). Group differences in perinatal outcomes were assessed using the chi-square test for categorical variables. For continuous variables, a one-way analysis of variance (ANOVA) was conducted, preceded by tests for normality and homogeneity of variances. The F-statistic evaluated overall group differences, with post-hoc pairwise comparisons to identify specific intergroup differences. All analyses were performed using SPSS Statistics (version 30.0.0.0, Armonk, NY, IBM Corp, 2024). Statistical significance was defined as p <0.05. RESULTS A total of 45179 singleton pregnancies were included. There were 54 (0.12%) stillbirths, of which 9 (16.7%) were SGA none were SGA< 3 rd centile 17 . There were 253 (0.56%) with the severe CAO, 659 (1.5%) with severe SGA (birthweight (6.3%) NNU admissions. Of the total cohort, 1453 (3.2%) were classified as ISUOG FGR (Group 1) and 966 (2.1%) as constitutionally SGA (Group 2); a further 2591 (5.7%) were classified as AGA with abnormal Dopplers but not meeting Delphi criteria (Group 3) and 2925 (6.5%) as AGA with ACGV < 10 th centile but not meeting Delphi criteria (Group 4), with 37244 (82.4%) classified as ‘normal’ AGA (Group 5). The relationship and overlaps between the groups is shown in Fig S1. The demographic and pregnancy characteristics of each phenotypic group are detailed in Table 1. The absolute risk of stillbirth and the severe CAO was broadly similar across all groups (Table 2); although the small numbers prevent comparison between FGR subtypes, there was no difference between the rate of stillbirth or the CAO between them and the ‘normal AGA’ group (p=0.782 and p=0.826, respectively). The majority of stillbirths (79.6%) and CAO (81%) occurred in the ‘normal’ AGA fetuses. Of the 9 (16.7%) stillbirths who were SGA at birth (<10 th centile 17 ), four were in the ‘normal AGA’ (Group 5) group, and therefore ‘undetected’. A further one had been classified as AGA with ACGV The risk of severe SGA (Table 2) at birth differed considerably between groups, with an OR of 27.1 (95% CI 22.4-32.8) with ISUOG FGR, but was also slightly increased with Groups 3 and 4 AGA FGR subtypes. Notably, the ‘normal’ AGA pregnancies contributed only 37.3% of all severely low 17 birthweight, implying a detection rate of the 36 week scan, using all SGA or FGR subtypes, of 62.7%. Among neonatal unit admissions, the majority (78.2%) were again accounted by ‘normal’ AGA babies. Table 3 shows intervention rates and also gestational age and birthweight. Intervention rates were higher in Groups 1 and 2, but the rates in the Groups 3 and 4 AGA FGR subgroups were little different from the normal AGA babies (Table 3 and Supplementary Table S1). DISCUSSION Main findings In this study we defined five fetal growth phenotypes at a universal late pregnancy scan, and assessed their association with adverse perinatal outcomes in a population of over 45000 singleton pregnancies. The principal finding is that the majority of severe clinical adverse outcomes occur in pregnancies classified at the 36 week scan as ‘normal’ AGA. That this is not entirely due to the poor scan performance is implied by the high detection rate of severe SGA at this scan, 18,19 if all SGA or FGR subtypes are classified as screen positives. Interpretation In established high-risk subgroups (Group 1 and 2), results reflect intervention. The ISUOG FGR have the highest risk of severe SGA with an OR of 27.1 (95% CI 22.4-32.8); 71.5% have their birth expedited with a mean gestational age at birth 12 days before the ‘normal’ AGA group. Their mortality is 0.14%, a figure that might be reduced further with the earlier birth that is probably appropriate in this group. 1,4 The constitutional SGA, with birth at gestation more in line with existing literature, are little heavier at birth. Their contribution to adverse outcomes undermines attempts to differentiate at 36 weeks between pathological and constitutional SGA. 20 Overall, these findings show that detected SGA babies have similar adverse outcomes rate to ‘normal AGA’ babies. In the cohort, only 16.7% of stillbirths were SGA; none had severe SGA. This is lower than usually quoted among term stillbirths 6 although SGA remains a significant problem. Detection might be improved by repeating the scan in selected women, for our previous analyses showed that pregnancies with an EFW between the 10 th and 20 th centile at the 36 week scan have a near 10-fold increase in the risk of severe SGA at birth (aOR 9.45; 95% CI 7.11– 12.54). 21 This is higher than the risk of severe SGA among our AGA suspected FGR groups (OR 3.26; 95% CI 2.42 - 4.38 and OR 2.56; 95% CI 1.88 – 3.49). The small contribution to adverse outcomes, the absence of severe SGA among stillbirths, and the relatively small proportion of even SGA<10 th centile (16.7%), all point to the limitations of size, whether ultrasound-estimated or birthweight, as a risk factor. Indeed, although an EFW 10 th -20 th centile was a risk factor for severe SGA in our previous analysis 21 , this risk did not extend to stillbirth (OR 1.35; 95% CI 0.53 – 3.41) or the more frequent composite severe adverse outcome (OR 1.05; 95% CI 0.64–1.70). The concept of FGR as opposed to size as a risk is widely supported. 1,8 Groups 3 and 4 were constructed (after exclusion of the Group 1) in line with existing literature suggesting increased risk: those where growth may be less than intended (AGA with ACGV <10 th centile) 16 and those where Doppler abnormalities suggest other placental unit dysfunction. 7 These two ‘pathological’ AGA groups have much lower rates of intervention than the SGA babies, indeed not dissimilar to the normal AGA group (Table S1). Yet they do not have a clearly higher risk of severe adverse outcomes than the normal AGA. This partly concurs with a recent randomized trial showing planned intervention based on CPR measurement near term in non SGA babies did not reduce mortality, although did reduce morbidity. 22 This and their sheer number (10% of all pregnancies), and therefore screen positives, undermines the potential of routinely using these parameters for decision making. The burden of risk for term stillbirth and the severe adverse outcome lies with pregnancies with normal and consistent biometry, and normal umbilical artery or cerebroplacental doppler by 36 weeks, and with babies of a ‘normal’ size at birth. This should not undermine the utility of systematic late pregnancy ultrasound screening for FGR as its potential benefits have been widely demonstrated, 18,19,23 but it is not enough. The issue for further term mortality reduction then is prediction of risk beyond 36 weeks. We have previously demonstrated the importance of pre-eclampsia and pre-existing diabetes but these accounted for only 10% of reported stillbirths. 21 Repeat ultrasound in a subset may detect more with severe SGA but the impact on adverse outcomes will be limited; similar strategies could be used to detect large for gestational age or accelerated growth, also known to confer some additional risk. 24,25 Indeed, comparison of growth patterns beyond 36 weeks in babies with normal and abnormal outcomes is urgently required. Nevertheless, risk prediction at term using currently available parameters remains poor. Strengths and limitations Although the majority of term perinatal mortality, severe neurological morbidity and severe morbidity has been reported to occur in infants apparently ”appropriately grown”, 26 the strength of our study is the prenatal phenotypic characterization of the AGA spectrum rather than considering the actual normal birthweight, which is only detected at birth. The detailed phenotypic classifications using established classification enabled robust comparisons across fetal growth patterns focusing on clinically adverse outcomes. Each fetus in our cohort was included in only one cluster and only a few exhibited concomitant ultrasonographic characteristics as shown in Supplementary Figure 1. Other strengths are the large cohort size, and the universal scan policy which eliminates selection bias. Intervention paradox, usually deemed as a study limitation, was used as a variable to examine its influence in attenuating associations with adverse events. Nevertheless, this does complicate the results. Intervention did occur, albeit to a limited extent in the AGA FGR groups, particularly group with abnormal Doppler indices, and this is reflected in the 2-3 days earlier gestation and slightly higher intervention rates. This limits inferences about the risk level in these groups. As with all such analyses, the accuracy of the scan will influence findings, but this reflects the ‘real world’. Finally, the analysis is constrained by the rarity of adverse perinatal outcomes at term and the inherent biases of the single-centre and retrospective design. CONCLUSION In a population universally screened for FGR around 36 weeks, most adverse outcomes occur in women with a normal result. This does not imply that the scan is ineffective, for the detection rate of severe SGA was high and the risk of adverse outcomes in pregnancies with accepted ‘abnormal’ findings was similar to those without. In the absence of better risk prediction, the biggest impact, at least on stillbirth, will currently only be from increased expedition of birth through routine early term induction of labour or CS. 27 This is difficult to achieve 28 and may have important adverse effects on the mother and indeed on the child in the long term ,29 Achieving a balance between these and the risk of stillbirth must be for parents and society to decide. Acknowledgements : None Disclosure : The authors report no conflict of interest CONTRIBUTION TO AUTHORSHIP ED’A: statistical analysis, study design, writing draft. CG: statistical analysis, study design, writing draft. CI study design, writing draft. CA study design, writing draft. MS: statistical analysis, writing draft. LI: concept, study design, writing draft. DETAILS OF ETHICS APPROVAL This study was approved by the Health Research Authority (IRAS project ID: 222260; REC reference: 17/SC/0374, updated July 2024). REFERENCES: 1. 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Ultrasound Obstet Gynecol. 2025 Apr;65(4):427-435. doi: 10.1002/uog.29218. Epub 2025 Mar 25. PMID: 40131231; PMCID: PMC11961102. 24. Robertson K, Vieira M, Impey L. Perinatal outcome of fetuses predicted to be large-for-gestational age on universal third-trimester ultrasound in non-diabetic pregnancy. Ultrasound Obstet Gynecol. 2024;63(1):98-104. doi:10.1002/uog.26305 25. Vieira MC, McCowan LME, North RA, et al. Antenatal risk factors associated with neonatal morbidity in large-for-gestational-age infants: an international prospective cohort study. Acta Obstet Gynecol Scand. 2018;97(8):1015-1024. doi:10.1111/aogs.13362 26. Triggs T, Crawford K, Hong J, Clifton V, Kumar S. The influence of birthweight on mortality and severe neonatal morbidity in late preterm and term infants: an Australian cohort study. Lancet Reg Health West Pac. 2024;45:101054. Published 2024 Apr 2. doi:10.1016/j.lanwpc.2024.101054 27. Middleton P, Shepherd E, Morris J, Crowther CA, Gomersall JC. Induction of labour at or beyond 37 weeks’ gestation. Cochrane Database Syst Rev. 2020;7(7):CD004945. 28. Taylor B, Cross‐Sudworth F, Rimmer M, et al. Induction of labour care in the UK: a cross‐sectional survey of maternity units. PLoS One. 2024;19(2):e0297857. 29. Alterman N, Johnson S, Carson C, et al. Gestational age at birth and academic attainment in primary and secondary school in England: evidence from a national cohort study. PLoS One. 2022;17(8):e0271952. Figure 1. Flowchart of the study population Table 1. Demographic and clinical pregnancy characteristics Table 2. Prevalence of adverse pregnancy outcomes according to fetal growth phenotypes Table 3. Prevalence of obstetric interventions and delivery outcomes according to fetal growth phenotypes Supplementary Material File (figure 1.docx) Download 35.57 KB File (table 1.docx) Download 17.17 KB File (table 2.docx) Download 30.37 KB File (table 3.docx) Download 31.08 KB Information & Authors Information Version history V1 Version 1 03 September 2025 Copyright This work is licensed under a Non Exclusive No Reuse License. Collection BJOG: An International Journal of Obstetrics and Gynaecology Keywords antenatal care doppler ultrasound fetal medicine fetal medicine: uteroplacental insufficiency pathology: perinatal risk management Authors Affiliations Elena D’Alberti 0000-0003-0526-6329 University of Oxford Nuffield Department of Women's & Reproductive Health View all articles by this author Chiara Granieri University of Oxford Nuffield Department of Women's & Reproductive Health View all articles by this author Christos Ioannou University of Oxford Nuffield Department of Women's & Reproductive Health View all articles by this author Christina Y.L. Aye University of Oxford Nuffield Department of Women's & Reproductive Health View all articles by this author Michael Shea John Radcliffe Hospital View all articles by this author Lawrence Impey 0000-0002-4462-112X [email protected] University of Oxford Nuffield Department of Women's & Reproductive Health View all articles by this author Metrics & Citations Metrics Article Usage 245 views 145 downloads .FvxKWukQNSOunydq8rnd { width: 100px; } Citations Download citation Elena D’Alberti, Chiara Granieri, Christos Ioannou, et al. Fetal phenotypes at a late third trimester scan: classification of risk and contribution to adverse outcomes. Authorea . 03 September 2025. DOI: https://doi.org/10.22541/au.175689562.29509572/v1 If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download. 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