Obstetric and pediatric growth charts for the detection of late-onset fetal growth restriction and neonatal adverse outcomes
-
Beatriz Fernandez-Rodriguez
, Concepción de Alba
, Alberto Galindo , David Recio , Cecilia Villalain , Carmen Rosa Pallas and Ignacio Herraiz
Abstract
Objectives
Late-onset fetal growth restriction (FGR) has heterogeneous prenatal and postnatal diagnostic criteria. We compared the prenatal and postnatal diagnosis of late-onset FGR and their ability to predict adverse perinatal outcomes.
Methods
Retrospective cohort study of 5442 consecutive singleton pregnancies that delivered beyond 34 + 0 weeks. Prenatal diagnosis of FGR was based on customized fetal growth standards and fetal Doppler while postnatal diagnosis was based on a birthweight <3rd percentile according to newborn charts (Olsen’s charts and Intergrowth 21st century programme). Perinatal outcomes were analyzed depending on whether the diagnosis was prenatal, postnatal or both.
Results
A total of 94 out of 5442 (1.7%) were diagnosed as late-onset FGR prenatally. Olsen’s chart and Intergrowth 21st chart detected that 125/5442 (2.3%) and 106/5442 (2.0%) of infants had a birthweight <3rd percentile, respectively. These charts identified 35/94 (37.2%) and 40/94 (42.6%) of the newborns with a prenatal diagnosis of late-onset FGR. Prenatally diagnosed late-onset FGR infants were at a higher risk for hypoglycemia, jaundice and polycythemia. Both prenatally and postnatally diagnosed as late-onset FGR had a higher risk for respiratory distress syndrome when compared to non-FGR. The higher risks for intensive care admission and composite adverse outcomes were observed in those with a prenatal diagnosis of late-onset FGR that was confirmed after birth.
Conclusions
Current definitions of pre- and postnatal late-onset FGR do not match in more than half of cases. Infants with a prenatal or postnatal diagnosis of this condition have an increased risk of neonatal morbidity even if these diagnoses are not coincident.
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: Due to the retrospective design of the study and the data anonymization it was unnecessary to have a signed informed consent from the patients.
Ethical approval: The local Ethics Committee approved the study (PI13/02405).
References
1. Seravalli, V, Baschat, AA. Uniform management approach to optimize outcome in fetal growth restriction. Obstet Gynecol Clin N Am 2015;42:275–88. https://doi.org/10.1016/j.ogc.2015.01.005.Search in Google Scholar PubMed
2. Beune, IM, Bloomfield, FH, Ganzevoort, W, Embleton, ND, Rozance, PJ, van Wassenaer-Leemhuis, AG, et al. Consensus based definition of growth restriction in the newborn. J Pediatr 2018;196:71–6.e1. https://doi.org/10.1016/j.jpeds.2017.12.059.Search in Google Scholar PubMed
3. Gordijn, SJ, Beune, IM, Ganzevoort, W. Building consensus and standards in fetal growth restriction studies. Best Pract Res Clin Obstet Gynaecol 2018;49:117–26. https://doi.org/10.1016/j.bpobgyn.2018.02.002.Search in Google Scholar PubMed
4. Parra-Saavedra, M, Simeone, S, Triunfo, S, Crovetto, F, Botet, F, Nadal, A, et al. Correlation between histological signs of placental underperfusion and perinatal morbidity in late-onset small-for-gestational-age fetuses. Ultrasound Obstet Gynecol 2015;45:149–55. https://doi.org/10.1002/uog.13415.Search in Google Scholar PubMed
5. Arcangeli, T, Thilaganathan, B, Hooper, R, Khan, KS, Bhide, A. Neurodevelopmental delay in small babies at term: a systematic review. Ultrasound Obstet Gynecol 2012;40:267–75. https://doi.org/10.1002/uog.11112.Search in Google Scholar PubMed
6. Baschat, AA. Planning management and delivery of the growth-restricted fetus. Best Pract Res Clin Obstet Gynaecol 2018;49:53–65. https://doi.org/10.1016/j.bpobgyn.2018.02.009.Search in Google Scholar PubMed
7. Figueras, F, Gratacós, E. Update on the diagnosis and classification of fetal growth restriction and proposal of a stage-based management protocol. Fetal Diagn Ther 2014;36:86–98. https://doi.org/10.1159/000357592.Search in Google Scholar PubMed
8. Thilaganathan, B. Ultrasound fetal weight estimation at term may do more harm than good. Ultrasound Obstet Gynecol 2018;52:5–8. https://doi.org/10.1002/uog.19110.Search in Google Scholar PubMed
9. Maso, G, Jayawardane, MA, Alberico, S, Piccoli, M, Senanayake, HM. The implications of diagnosis of small for gestational age fetuses using European and South Asian growth charts: an outcome-based comparative study. Sci World J 2014;2014:474809. https://doi.org/10.1155/2014/474809.Search in Google Scholar PubMed PubMed Central
10. Malin, GL, Morris, RK, Riley, R, Teune, MJ, Khan, KS. When is birthweight at term abnormally low? A systematic review and meta-analysis of the association and predictive ability of current birthweight standards for neonatal outcomes. BJOG 2014;121:515–26. https://doi.org/10.1111/1471-0528.12517.Search in Google Scholar PubMed PubMed Central
11. Parra-Saavedra, M, Crovetto, F, Triunfo, S, Savchev, S, Peguero, A, Nadal, A, et al. Association of Doppler parameters with placental signs of underperfusion in late onset small-for-gestational-age pregnancies. Ultrasound Obstet Gynecol 2014;44:330–7. https://doi.org/10.1002/uog.13358.Search in Google Scholar PubMed
12. Oros, D, Figueras, F, Cruz-Martinez, R, Meler, E, Munmany, M, Gratacos, E. Longitudinal changes in uterine, umbilical and fetal cerebral Doppler indices in late-onset small-for-gestational age fetuses. Ultrasound Obstet Gynecol 2011;37:191–5. https://doi.org/10.1002/uog.7738.Search in Google Scholar PubMed
13. Garcia-Simon, R, Figueras, F, Savchev, S, Fabre, E, Gratacos, E, Oros, D. Cervical condition and fetal cerebral Doppler as determinants of adverse perinatal outcome after labor induction for late-onset small-for-gestational-age fetuses. Ultrasound Obstet Gynecol 2015;46:713–7. https://doi.org/10.1002/uog.14807.Search in Google Scholar PubMed
14. Mureșan, D, Rotar, IC, Stamatian, F. The usefulness of fetal Doppler evaluation in early versus late onset intrauterine growth restriction. Review of the literature. Med Ultrason 2016;18:103–9. https://doi.org/10.11152/mu.2013.2066.181.dop.Search in Google Scholar PubMed
15. Man, J, Hutchinson, JC, Ashworth, M, Heazell, AE, Levine, S, Sebire, NJ. Effects of intrauterine retention and postmortem interval on body weight following intrauterine death: implications for assessment of fetal growth restriction at autopsy. Ultrasound Obstet Gynecol 2016;48:574–8. https://doi.org/10.1002/uog.16018.Search in Google Scholar PubMed
16. Herraiz, I, Simón, E, Gómez-Arriaga, PI, Martínez-Moratalla, JM, García-Burguillo, Jiménez, EA, Galindo, A. Angiogenesis-related biomarkers (sFlt-1/PLGF) in the prediction and diagnosis of placental dysfunction: an approach for clinical integration. Int J Mol Sci 2015;16:19009–26. https://doi.org/10.3390/ijms160819009.Search in Google Scholar PubMed PubMed Central
17. Herraiz, I, Simón, E, Gómez-Arriaga, PI, Quezada, MS, García-Burguillo, A, López-Jiménez, EA, et al. Clinical implementation of the sFlt-1/PlGF ratio to identify preeclampsia and fetal growth restriction: a prospective cohort study. Pregnancy Hypertens 2018;13:279–85. https://doi.org/10.1016/j.preghy.2018.06.017.Search in Google Scholar PubMed
18. Zeisler, H, Llurba, E, Chantraine, F, Vatish, M, Staff, AC, Sennström, M, et al. Predictive value of the sFlt-1:PlGF ratio in women with suspected preeclampsia. N Engl J Med 2016;374:13–22. https://doi.org/10.1056/nejmoa1414838.Search in Google Scholar PubMed
19. Method for estimating due date. Committee opinion No. 611. American College of Obstetrics and Gynecology. Obstet Gynecol 2014;124:863–6 https://doi.org/10.1097/01.AOG.0000454932.15177.be.Search in Google Scholar PubMed
20. 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. https://doi.org/10.1016/0002-9378(85)90298-4.Search in Google Scholar PubMed
21. Sweet, DG, Carnielli, V, Greisen, G, Hallman, M, Ozek, E, Te Pas, A, et al. European consensus guidelines on the management of neonatal respiratory distress syndrome in preterm infants–2013 update. Neonatology 2013;103:353–68. https://doi.org/10.1159/000349928.Search in Google Scholar PubMed
22. American Academy of Pediatrics Subcommittee on Hyperbilirubinemia. Management of hyperbilirubinemia in the newborn infant 35 or more weeks of gestation. Pediatrics 2004;114:297–316 https://doi.org/10.1542/peds.114.1.297.Search in Google Scholar PubMed
23. Boers, KE, van Wyk, L, van der Post, JA, Kwee, A, van Pampus, MG, Spaanderdam, ME, et al. Neonatal morbidity after induction vs expectant monitoring in intrauterine growth restriction at term: a subanalysis of the DIGITAT RCT. Am J Obstet Gynecol 2012;206:344–7. https://doi.org/10.1016/j.ajog.2012.01.015.e1.Search in Google Scholar PubMed
24. Olsen, IE, Groveman, S, Lawson, ML, Clark, R, Zemel, B. New intrauterine growth curves based on United States data. Pediatrics 2010;125:e214–24. https://doi.org/10.1542/peds.2009-0913.Search in Google Scholar PubMed
25. Villar, J, Cheikh Ismail, L, Victora, CG, Ohuma, E, Bertino, E, Altman, D, et al. For the international fetal and newborn growth consortium for the 21st century (INTERGROWTH-21st). International standards for newborn weight, length, and head circumference by gestational age and sex: the newborn cross-sectional study of the INTERGROWTH-21st project. Lancet 2014;384:857–68. https://doi.org/10.1016/s0140-6736(14)60932-6.Search in Google Scholar
26. Villar, J, Giuliani, F, Bhutta, Z, Bertino, E, Ohuma, EO, Cheikh Ismail, L, et al. For the international fetal and newborn growth consortium for the 21st century (INTERGROWTH-21st). Postnatal growth standards for preterm infants: the preterm postnatal follow-up study of the INTERGROWTH-21st project. Lancet Glob Health 2015;3:e681–91. https://doi.org/10.1016/s2214-109x(15)00163-1.Search in Google Scholar PubMed
27. Parra-Saavedra, M, Crovetto, F, Triunfo, S, Savchev, S, Peguero, A, Nadal, A, et al. Placental findings in late-onset SGA births without Doppler signs of placental insufficiency. Placenta 2013;34:1136–41. https://doi.org/10.1016/j.placenta.2013.09.018.Search in Google Scholar PubMed
28. Savchev, S, Figueras, F, Sanz-Cortes, M, Cruz-Lemini, M, Triunfo, S, Botet, F, et al. Evaluation of an optimal gestational age cut-off for the definition of early- and late-onset fetal growth restriction. Fetal Diagn Ther 2014;36:99–105. https://doi.org/10.1159/000355525.Search in Google Scholar PubMed
29. Mateus, J, Newman, RB, Zhang, C, Pugh, SJ, Grewal, J, Kim, S, et al. Fetal growth patterns in pregnancy-associated hypertensive disorders: NICHD Fetal Growth Studies. Am J Obstet Gynecol 2019;221:635–16. https://doi.org/10.1016/j.ajog.2019.06.028.e1.Search in Google Scholar PubMed PubMed Central
30. Villalaín, C, Herraiz, I, Quezada, MS, Gómez-Arriaga, PI, Gómez-Montes, E, Galindo, A. Fetal biometry and Doppler study for the assessment of perinatal outcome in stage I late-onset fetal growth restriction. Fetal Diagn Ther 2018;44:264–70. https://doi.org/10.1159/000485124.Search in Google Scholar PubMed
31. Parra-Saavedra, M, Crovetto, F, Triunfo, S, Savchev, S, Parra, G, Sanz, M, et al. Added value of umbilical vein flow as a predictor of perinatal outcome in term small-for-gestational-age fetuses. Ultrasound Obstet Gynecol 2013;42:189–95. https://doi.org/10.1002/uog.12380.Search in Google Scholar PubMed
32. 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 2020;55:793–8. https://doi.org/10.1002/uog.20406.Search in Google Scholar PubMed
33. Verkauskiene, R, Figueras, F, Deghmoun, S, Chevenne, D, Gardosi, J, Levy-Marchal, M. Birth weight and long-term metabolic outcomes: does the definition of smallness matter?. Horm Res 2008;70:309–15. https://doi.org/10.1159/000157878.Search in Google Scholar PubMed
34. Chiossi, G, Pedroza, C, Costantine, MM, Truong, VTT, Gargano, G, Saade, GR. Customized vs population-based growth charts to identify neonates at risk of adverse outcome: systematic review and Bayesian meta-analysis of observational studies. Ultrasound Obstet Gynecol 2017;50:156–66. https://doi.org/10.1002/uog.17381.Search in Google Scholar PubMed
35. Crispi, F, Miranda, J, Gratacós, E. Long-term cardiovascular consequences of fetal growth restriction: biology, clinical implications, and opportunities for prevention of adult disease. Am J Obstet Gynecol 2018;218:S869–79. https://doi.org/10.1016/j.ajog.2017.12.012.Search in Google Scholar PubMed
36. Rizzo, G, Mattioli, C, Mappa, I, Bitsadze, V, Khizroeva, J, Słodki, M, et al. Hemodynamic factors associated with fetal cardiac remodeling in late fetal growth restriction: a prospective study. J Perinat Med 2019;47:683–8. https://doi.org/10.1515/jpm-2019-0217.Search in Google Scholar PubMed
37. Odibo, AO, Nwabuobi, C, Odibo, L, Leavitt, K, Obican, S, Tuuli, MG. Customized fetal growth standard compared with the INTERGROWTH-21st century standard at predicting small-for-gestational-age neonates. Acta Obstet Gynecol Scand 2018;97:1381–7. https://doi.org/10.1111/aogs.13394.Search in Google Scholar PubMed
38. Kabiri, D, Romero, R, Gudicha, DW, Hernandez-Andrade, E, Pacora, P, Benshalom-Tirosh, N, et al. Prediction of adverse perinatal outcome by fetal biometry: comparison of customized and population-based standards. Ultrasound Obstet Gynecol 2020;55:177–88. https://doi.org/10.1002/uog.20299.Search in Google Scholar PubMed PubMed Central
39. Boers, KE, van Wyk, L, van der Post, JA, Kwee, A, van Pampus, MG, Spaanderdam, ME, et al. Neonatal morbidity after induction vs expectant monitoring in intrauterine growth restriction at term: a subanalysis of the DIGITAT RCT. Am J Obstet Gynecol 2012;206:344–7. https://doi.org/10.1016/j.ajog.2012.01.015.e1.Search in Google Scholar PubMed
40. Quênya, I, Araujo, E, Machado, L, Galvão, C, Paranaíba, V, Borges, A. Perinatal outcomes of fetuses with early growth restriction, late growth restriction, small for gestational age, and adequate for gestational age. Rev Bras Ginecol Obstet 2019;41:688–96. https://doi.org/10.1055/s-0039-1697987.Search in Google Scholar PubMed
41. Fernandez-Rodriguez, B, de Alba, C, Villalain, C, Pallás, CR, Galindo, A, Herraiz, I. Obstetric and pediatric growth charts for the detection of fetal growth restriction and neonatal adverse outcomes in preterm newborns before 34 weeks of gestation. J Matern Fetal Neonatal Med 2019;9:1–8. https://doi.org/10.1080/14767058.2019.1626368.Search in Google Scholar PubMed
42. Sharma, D, Shastri, S, Sharma, P. Intrauterine growth restriction: antenatal and postnatal aspects. Clin Med Insights Pediatr 2016;10:67–83. https://doi.org/10.4137/cmped.s40070.Search in Google Scholar
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/jpm-2020-0210).
© 2020 Walter de Gruyter GmbH, Berlin/Boston
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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
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