The ability of various cerebroplacental ratio thresholds to predict adverse neonatal outcomes in term fetuses exhibiting late-onset fetal growth restriction
Abstract
Objectives
Our primary aim was to evaluate the ability of various cerebroplacental ratio (CPR) reference values suggested by the Fetal Medicine Foundation to predict adverse neonatal outcomes in term fetuses exhibiting late-onset fetal growth restriction (LOFGR). Our secondary aim was to evaluate the effectiveness of other obstetric Doppler parameters used to assess fetal well-being in terms of predicting adverse neonatal outcomes.
Methods
This was a retrospective cohort study of 317 pregnant women diagnosed with LOFGR at 37–40 weeks of gestation between January 1, 2016, and September 1, 2019. Receiver operating characteristic (ROC) curves were drawn to determine the predictive performance of CPR <1, CPR <5th or <10th percentile, and umbilical artery pulsatility (PI) >95th percentile in terms of predicting adverse neonatal outcomes.
Results
Pregnant women exhibiting LOFGR who gave birth in our clinic during the study period at a mean of 38 gestational weeks (minimum 37+0; maximum 40+6 weeks); the median CPR was 1.51 [interquartile range (IQR) 1.12–1.95] and median birthweight 2,350 g (IQR 2,125–2,575 g). The CPR <5th percentile best predicted adverse neonatal outcomes [area under the curve (AUC) 0.762, 95% confidence interval (CI) 0.672–0.853, p<0.0001] and CPR <1 was the worst predictor (AUC 0.630, 95% CI 0.515–0.745, p=0.021). Of other Doppler parameters, neither the umbilical artery systole/diastole ratio nor the mid-cerebral artery to peak systolic velocity ratio (MCA–PSV) predicted adverse neonatal outcomes (AUC 0.598, 95% CI 0.480–0.598, p=0.104; AUC 0.521, 95% CI 0.396–0.521, p=0.744 respectively).
Conclusions
The CPR values below the 5th percentile better predicted adverse neonatal outcomes in pregnancies complicated by LOFGR than the UA PI and CPR <1 by using Fetal Medicine Foundation reference ranges.
Acknowledgments
The English in this document has been checked by at least two professional editors, both native speakers of English. For a certificate, please see: http://www.textcheck.com/certificate/3XBGPU.
Research funding: None declared.
Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.
Competing interests: Authors state no conflict of interest.
Informed consent: Informed consent was obtained from all individuals included in this study.
Ethical approval: The institutional Ethics Committee approved this retrospective cohort study (no. 2019/7-13).
References
1. Figueras, F, Caradeux, J, Crispi, F, Eixarch, E, Peguero, A, Gratacos, E. Diagnosis and surveillance of late-onset fetal growth restriction. Am J Obstet Gynecol 2018;218:S790–802. e1. https://doi.org/10.1016/j.ajog.2017.12.003.Search in Google Scholar
2. Society for Maternal-Fetal Medicine (SMFM), Martins, JG, Biggio, JR, Abuhamad, A. Society for maternal-fetal medicine (SMFM) consult series #52: diagnosis and management of fetal growth restriction. Am J Obstet Gynecol 2020 May 11. pii: S0002-9378(20)30535-4. [Epub ahead of print].Search in Google Scholar
3. Vollgraff Heidweiller-Schreurs, CA, De Boer, MA, Heymans, MW, Schoonmade, LJ, Bossuyt, PMM, Mol, BWJ, et al. Prognostic accuracy of cerebroplacental ratio and middle cerebral artery Doppler for adverse perinatal outcome: systematic review and meta-analysis. Ultrasound Obstet Gynecol 2018;51:313–22. https://doi.org/10.1002/uog.18809.Search in Google Scholar
4. Morales-Rosello, J, Khalil, A, Morlando, M, Bhide, A, Papageorghiou, A, Thilaganathan, B. Poor neonatal acid-base status in term fetuses with low cerebroplacental ratio. Ultrasound Obstet Gynecol 2015;45:156–61. https://doi.org/10.1002/uog.14647.Search in Google Scholar
5. Oros, D, Figueras, F, Cruz-Martinez, R, Padilla, N, Meler, E, Hernandez-Andrade, E, et al. Middle versus anterior cerebral artery Doppler for the prediction of perinatal outcome and neonatal neurobehavior in term small-for-gestational-age fetuses with normal umbilical artery Doppler. Ultrasound Obstet Gynecol 2010;35:456–61. https://doi.org/10.1002/uog.7588.Search in Google Scholar
6. Akolekar, R, Ciobanu, A, Zingler, E, Syngelaki, A, Nicolaides, KH. Routine assessment of cerebroplacental ratio at 35–37 weeks’ gestation in the prediction of adverse perinatal outcome. Am J Obstet Gynecol 2019;221:65.e1–65.e18. https://doi.org/10.1016/j.ajog.2019.03.002.Search in Google Scholar
7. DeVore, GR. The importance of the cerebroplacental ratio in the evaluation of fetal well-being in SGA and AGA fetuses. Am J Obstet Gynecol 2015;213:5–15. https://doi.org/10.1016/j.ajog.2015.05.024.Search in Google Scholar
8. Gordijn, SJ, Beune, IM, Thilaganathan, B, Papageorghiou, A, Baschat, AA, Baker, PN, et al. Consensus definition of fetal growth restriction: a Delphi procedure. Ultrasound Obstet Gynecol 2016;48:333–9. https://doi.org/10.1002/uog.15884.Search in Google Scholar
9. Salomon, LJ, Alfirevic, Z, Da Silva Costa, F, Deter, RL, Figueras, F, Ghi, T, et al. ISUOG Practice Guidelines: ultrasound assessment of fetal biometry and growth. Ultrasound Obstet Gynecol 2019;53:715–23. https://doi.org/10.1002/uog.20272.Search in Google Scholar
10. Oros, D, Ruiz-Martinez, S, Staines-Urias, E, Conde-Agudelo, A, Villar, J, Fabre, E, et al. Reference ranges for Doppler indices of umbilical and fetal middle cerebral arteries and cerebroplacental ratio: systematic review. Ultrasound Obstet Gynecol 2019;53:454–64. https://doi.org/10.1002/uog.20102.Search in Google Scholar
11. Flatley, C, Kumar, S, Greer, RM. Reference centiles for the middle cerebral artery and umbilical artery pulsatility index and cerebro-placental ratio from a low-risk population-a Generalised Additive Model for Location, Shape and Scale (GAMLSS) approach. J Matern Fetal Neonatal Med 2019;32:2338–45. https://doi.org/10.1080/14767058.2018.1432590.Search in Google Scholar
12. Ciobanu, A, Wright, A, Syngelaki, A, Wright, D, Akolekar, R, Nicolaides, KH. Fetal Medicine Foundation reference ranges for umbilical artery and middle cerebral artery pulsatility index and cerebroplacental ratio. Ultrasound Obstet Gynecol 2019;53:465–72. https://doi.org/10.1002/uog.20157.Search in Google Scholar
13. Khalil, AA, Morales-Rosello, J, Elsaddig, M, Khan, N, Papageorghiou, A, Bhide, A, et al. The association between fetal Doppler and admission to neonatal unit at term. Am J Obstet Gynecol 2015;213:57.e1–57.e7. https://doi.org/10.1016/j.ajog.2014.10.013.Search in Google Scholar
14. Khalil, AA, Morales-Rosello, J, Morlando, M, Hannan, H, Bhide, A, Papageorghiou, A, et al. Is fetal cerebroplacental ratio an independent predictor of intrapartum fetal compromise and neonatal unit admission?. Am J Obstet Gynecol 2015;213:54.e1–54.e10. https://doi.org/10.1016/j.ajog.2014.10.024.Search in Google Scholar
15. Flood, K, Unterscheider, J, Daly, S, Geary, MP, Kennelly, MM, McAuliffe, FM, et al. The role of brain sparing in the prediction of adverse outcomes in intrauterine growth restriction: results of the multicenter PORTO Study. Am J Obstet Gynecol 2014;211:288. https://doi.org/10.1016/j.ajog.2014.05.008. e1–e5.Search in Google Scholar
16. Prior, T, Mullins, E, Bennett, P, Kumar, S. Prediction of intrapartum fetal compromise using the cerebroumbilical ratio: a prospective observational study. Am J Obstet Gynecol 2013;208:124. https://doi.org/10.1016/j.ajog.2012.11.016. e1–e6.Search in Google Scholar
17. Bligh, LN, Alsolai, AA, Greer, RM, Kumar, S. Cerebroplacental ratio thresholds measured within 2 weeks before birth and risk of Cesarean section for intrapartum fetal compromise and adverse neonatal outcome. Ultrasound Obstet Gynecol 2018;52:340–6. https://doi.org/10.1002/uog.17542.Search in Google Scholar
18. Cruz‐Martinez, R, Savchev, S, Cruz‐Lemini, M, Mendez, A, Gratacos, E, Figueras, F. Clinical utility of third‐trimester uterine artery Doppler in the prediction of brain hemodynamic deterioration and adverse perinatal outcome in small‐for gestational‐age fetuses. Ultrasound Obstet Gynecol 2015;45:273–8.10.1002/uog.14706Search in Google Scholar PubMed
19. Frusca, T, Todros, T, Lees, C, Bilardo, CM. Outcome in early-onset fetal growth restriction is best combining computerized fetal heart rate analysis with ductus venosus Doppler: insights from the trial of umbilical and fetal flow in Europe. Am J Obstet Gynecol 2018;218:S783–9. https://doi.org/10.1016/j.ajog.2017.12.226.Search in Google Scholar
20. Rizzo, G, Mappa, I, Bitsadze, V, Słodki, M, Khizroeva, J, Makatsariya, A, et al. Role of Doppler ultrasound at time of diagnosis of late-onset fetal growth restriction in predicting adverse perinatal outcome: prospective cohort study. Ultrasound Obstet Gynecol 2019 Jul 25. https://doi.org/10.1002/uog.20406. [Epub ahead of print].Search in Google Scholar
21. Ruiz-Martinez, S, Papageorghiou, AT, Staines-Urias, E, Villar, J, de Agüero, RG, Oros, D. Clinical impact of Doppler reference charts to manage fetal growth restriction: need for standardization. Ultrasound Obstet Gynecol 2019 Jun 25. https://doi.org/10.1002/uog.20380. [Epub ahead of print].Search in Google Scholar
22. Ebbing, C, Rasmussen, S, Kiserud, T. Middle cerebral artery blood flow velocities and pulsatility index and the cerebroplacental pulsatility ratio: longitudinal reference ranges and terms for serial measurements. Ultrasound Obstet Gynecol 2007;30:287–96. https://doi.org/10.1002/uog.4088.Search in Google Scholar
23. Parra-Cordero, M, Lees, C, Missfelder-Lobos, H, Seed, P, Harris, C. Fetal arterial and venous Doppler pulsatility index and time averaged velocity ranges. Prenat Diagn 2007;27:1251–7. https://doi.org/10.1002/pd.1868.Search in Google Scholar
24. Bahlmann, F, Fittschen, M, Reinhard, I, Wellek, S, Puhl, A. Blood flow velocity waveforms of the umbilical artery in a normal population: reference values from 18 weeks to 42 weeks of gestation. Ultraschall Med 2012;33:E80–87. https://doi.org/10.1055/s-0031-1299294.Search in Google Scholar
25. Morales-Roselló, J, Khalil, A, Morlando, M, Hervás-Marín, D, Perales-Marín, A. Doppler reference values of the fetal vertebral and middle cerebral arteries, at 19–41 weeks gestation. J Matern Fetal Neonatal Med 2015;28:338–43.10.3109/14767058.2014.916680Search in Google Scholar PubMed
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Articles in the same Issue
- Frontmatter
- Review
- Methods of detection and prevention of preterm labour and the PAMG-1 detection test: a review
- Corner of Academy
- Long term alterations of growth after antenatal steroids in preterm twin pregnancies
- Original Articles – Obstetrics
- SARS-CoV-2 in pregnancy: maternal and perinatal outcome data of 34 pregnant women hospitalised between May and October 2020
- Comparison of hematological parameters and perinatal outcomes between COVID-19 pregnancies and healthy pregnancy cohort
- The effect of mask use on maternal oxygen saturation in term pregnancies during the COVID-19 process
- Risk factors for pregnancy-associated venous thromboembolism in Singapore
- Does the length of second stage of labour or second stage caesarean section in nulliparous women increase the risk of preterm birth in subsequent pregnancies?
- Reference range for C1-esterase inhibitor (C1 INH) in the third trimester of pregnancy
- Termination of pregnancy following a Down Syndrome diagnosis: decision-making process and influential factors in a Muslim but secular country, Turkey
- High dose vs. low dose oxytocin for labor augmentation: a systematic review and meta-analysis of randomized controlled trials
- Extremely high levels of alkaline phosphatase and pregnancy outcome: case series and review of the literature
- Cervical elastography strain ratio and strain pattern for the prediction of a successful induction of labour
- Original Articles – Fetus
- CD34 immunostain increases sensitivity of the diagnosis of fetal vascular malperfusion in placentas from ex-utero intrapartum treatment
- The ability of various cerebroplacental ratio thresholds to predict adverse neonatal outcomes in term fetuses exhibiting late-onset fetal growth restriction
- Obstetric and pediatric growth charts for the detection of late-onset fetal growth restriction and neonatal adverse outcomes
- Original Articles – Neonates
- Bacterial stability with freezer storage of human milk
- Protein and genetic expression of CDKN1C and IGF2 and clinical features related to human umbilical cord length
- Short Communication
- A considerable asymptomatic proportion and thromboembolism risk of pregnant women with COVID-19 infection in Wuhan, China