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Published:October 10, 2018DOI:https://doi.org/10.1016/j.ajog.2018.10.007

      The Issue

      Fetal growth restriction is an indicator of placental insufficiency and is strongly associated with adverse perinatal outcome. There is a point that the recent dominance in the medical literature about which reference charts to use and dichotomization of fetal size at the 10th percentile overlooks the fact there is not a single cut-off in any growth chart that acts as an absolute divider between high and low risk for adverse outcome. Thus, the collective goal of all researchers to identify, monitor and effectively manage growth-restricted fetuses is better served by replacing dichotomisation of normal versus abnormal fetal growth at the 10th percentile by interpretation of fetal size in context with other known parameters of fetal risk - all as continuous parameters. The use of prospective comprehensive datasets should facilitate better risk assessment for the individual fetus, to help direct effective and appropriate interventions. The counterpoint is that the debate about which growth standard to use was necessary and has been settled through evidence that size, and therefore growth, need customized limits to allow adjustment for constitutional variation, and to help distinguish between normal and abnormal growth. Implementation of a more precise standard has led to better detection of fetuses that are at risk due to growth restriction, improved application of additional investigations, enhanced clinical confidence in management including timely delivery, and ultimately increased prevention of adverse outcomes.
      In the February 2018 issue of the American Journal of Obstetrics and Gynecology, important articles were published that summarized some of the major issues in fetal growth restriction (FGR).
      • Romero R.
      • Kingdom J.
      • Deter R.
      • Lee W.
      • Vintzileos A.
      Fetal growth: evaluation and management.
      Although all researchers undoubtedly share the same overall goal to improve prevention, detection, and outcomes of FGR, we think that the issue of which reference chart should be used is predominant. We argue that this impasse distracts from the actual issue and wastes both clinical and academic resources. In this article, we highlight how the focus on fetal size as a proxy for fetal growth and adequate placental nutrition has been oversimplified as “above” or “below” the 10th percentile to distinguish between apparently normal and abnormal fetal growth. This dichotomization results in erroneous underdiagnosis of growth-restricted fetuses among those that apparently are grown normally with the risk of adverse outcomes because of lack of medical attention. Conversely, among constitutionally small fetuses, it leads to overdiagnosis of FGR and risk from unnecessary obstetric intervention. FGR can result from any disease that affects placental function and is associated with significant adverse short- and long-term outcomes.
      • Crispi F.
      • Miranda J.
      • Gratacos E.
      Long-term cardiovascular consequences of fetal growth restriction: biology, clinical implications, and opportunities for prevention of adult disease.
      • Figueras F.
      • Caradeux J.
      • Crispi F.
      • Eixarch E.
      • Peguero A.
      • Gratacos E.
      Diagnosis and surveillance of late-onset fetal growth restriction.
      • Caradeux J.
      • Martinez-Portilla R.J.
      • Basuki T.R.
      • Kiserud T.
      • Figueras F.
      Risk of fetal death in growth-restricted fetuses with umbilical and/or ductus venosus absent or reversed end-diastolic velocities before 34 weeks of gestation: a systematic review and meta-analysis.
      Accordingly, adequate detection and risk stratification is of paramount importance to guide perinatal care. With >10,000 citations on “prenatal diagnosis” or “definition” of FGR in current medical literature, we have achieved little progress beyond the initial landmark observation that fetal size apparently is expressed optimally by ascribing a percentile to its estimate.
      • Lubchenco L.O.
      • Hansman C.
      • Dressler M.
      • Boyd E.
      Intrauterine growth as estimated from liveborn birth-weight data at 24 to 42 weeks of gestation.
      This article argues that we should progress beyond fetal size assessment alone and undertake a more comprehensive risk assessment with the use of contemporary techniques.

      Which fetal growth chart?

      Population-based reference charts

      Population-based fetal size charts are created from retrospective datasets and by nature are descriptive and show how the fetuses in the observed population have grown. These references are skewed at the extremes of gestation where pathologic conditions, such as preeclampsia and preterm birth, are concentrated, because these abnormal pregnancies usually are not excluded in their development.
      • Lubchenco L.O.
      • Hansman C.
      • Dressler M.
      • Boyd E.
      Intrauterine growth as estimated from liveborn birth-weight data at 24 to 42 weeks of gestation.
      • Kloosterman G.J.
      On intrauterine growth - the significance of prenatal care.
      This still holds true for more recent descriptive reference charts.
      • Visser G.H.
      • Eilers P.H.
      • Elferink-Stinkens P.M.
      • Merkus H.M.
      • Wit J.M.
      New Dutch reference curves for birthweight by gestational age.

      Customized fetal growth assessment

      To overcome some of the methodologic drawbacks of population-based growth charts, Gardosi et al
      • Gardosi J.
      • Chang A.
      • Kalyan B.
      • Sahota D.
      • Symonds E.M.
      Customised antenatal growth charts.
      constructed growth charts that attempt mathematically to predict normal variation in growth at term. This group introduced the idea of customization by correcting for maternal characteristics that individualize the expected growth potential of the fetus.
      • Gardosi J.
      • Francis A.
      • Turner S.
      • Williams M.
      Customized growth charts: rationale, validation and clinical benefits.
      Many variables have been used for correction such as fetal gender, maternal height, weight, ethnicity, and parity. At first glance, ethnicity seems to be an intuitive variable for customization, but ethnicity is often associated with poorer socioeconomic status that may be the determinant for adverse perinatal outcomes.
      • Poeran J.
      • Maas A.F.
      • Birnie E.
      • Denktas S.
      • Steegers E.A.
      • Bonsel G.J.
      Social deprivation and adverse perinatal outcomes among Western and non-Western pregnant women in a Dutch urban population.
      Definition and self-reported categorization of race is difficult, particularly in a multiethnic and continuously mingling society.
      • Lockie E.
      • McCarthy E.
      • Hui L.
      • Churilov L.
      • Walker S.P.
      Feasibility of using self-reported ethnicity in pregnancy according to the gestation related optimal weight classification: a cross-sectional study.
      Additionally, how much can change in transition from a generation of severe deprivation to a well-nourished and healthy generation is not known. We suggest that individual variables should be assessed comprehensively for their individual putative merits and their well-known existing relationship with adverse outcomes. In the available datasets of second and third generation migrants, we can test how many generations are required for adverse effects to subside. Similar interactions may be observed for maternal weight and parity, but fetal gender and maternal height may have a stronger argument to be used in customization.
      • Visser G.H.
      • Eilers P.H.
      • Elferink-Stinkens P.M.
      • Merkus H.M.
      • Wit J.M.
      New Dutch reference curves for birthweight by gestational age.
      Even though there may be an academic discussion about the concept of customization, the initiative to use back-calculated growth charts from a healthy term cohort and serially to plot growth assessments in a systematic manner have significantly improved awareness about growth and identification of fetuses at risk.
      • Gardosi J.
      • Francis A.
      • Turner S.
      • Williams M.
      Customized growth charts: rationale, validation and clinical benefits.
      • De Jong C.L.
      • Gardosi J.
      • Dekker G.A.
      • Colenbrander G.J.
      • Van Geijn H.P.
      Application of a customised birthweight standard in the assessment of perinatal outcome in a high risk population.
      • Gardosi J.
      • Francis A.
      Controlled trial of fundal height measurement plotted on customised antenatal growth charts.

      Prescriptive growth standards

      To a certain extent, healthy populations across the world are expected to have similar fetal growth, because only 1 species of humans exists without large phylogenetic differences.
      • Horikoshi M.
      • Beaumont R.N.
      • Day F.R.
      • et al.
      Genome-wide associations for birth weight and correlations with adult disease.
      Recent initiatives prospectively have followed healthy uncomplicated pregnancies with sequential ultrasound scans to develop prescriptive growth standards and to define how a healthy fetus grows.
      • Verburg B.O.
      • Steegers E.A.
      • De Ridder M.
      • et al.
      New charts for ultrasound dating of pregnancy and assessment of fetal growth: longitudinal data from a population-based cohort study.
      • Papageorghiou A.T.
      • Ohuma E.O.
      • Altman D.G.
      • et al.
      International standards for fetal growth based on serial ultrasound measurements: the Fetal Growth Longitudinal Study of the INTERGROWTH-21st Project.
      • Kiserud T.
      • Piaggio G.
      • Carroli G.
      • et al.
      The World Health Organization fetal growth charts: a multinational longitudinal study of ultrasound biometric measurements and estimated fetal weight.
      • Kiserud T.
      • Benachi A.
      • Hecher K.
      • et al.
      The World Health Organization fetal growth charts: concept, findings, interpretation, and application.
      • Grantz K.L.
      • Hediger M.L.
      • Liu D.
      • Buck Louis G.M.
      Fetal growth standards: the NICHD fetal growth study approach in context with INTERGROWTH-21st and the World Health Organization Multicentre Growth Reference Study.
      In the Intergrowth-21 study that was performed in 8 different countries, measurement variation between countries was significantly smaller than within-population variation.
      • Papageorghiou A.T.
      • Ohuma E.O.
      • Altman D.G.
      • et al.
      International standards for fetal growth based on serial ultrasound measurements: the Fetal Growth Longitudinal Study of the INTERGROWTH-21st Project.
      • Papageorghiou A.T.
      • Kennedy S.H.
      • Salomon L.J.
      • et al.
      The INTERGROWTH-21(st) fetal growth standards: toward the global integration of pregnancy and pediatric care.
      This uniformity suggests that prescriptive growth charts are the gold standard. However, there is persistent significant variation in fetal growth within each population when environmental constraints are not controlled for adequately. Apparently, these factors have a significant adverse influence on fetal growth and not all fetuses grow the same.
      • Kiserud T.
      • Benachi A.
      • Hecher K.
      • et al.
      The World Health Organization fetal growth charts: concept, findings, interpretation, and application.
      • Grantz K.L.
      • Hediger M.L.
      • Liu D.
      • Buck Louis G.M.
      Fetal growth standards: the NICHD fetal growth study approach in context with INTERGROWTH-21st and the World Health Organization Multicentre Growth Reference Study.

      The way forward

      Obviously, these approaches are conceptually different, and protagonists of either approach are in fundamental disagreement. Much effort is put into comparing how either approach performs retrospectively in large datasets.
      • Francis A.
      • Hugh O.
      • Gardosi J.
      Customized vs INTERGROWTH-21(st) standards for the assessment of birthweight and stillbirth risk at term.
      These analyses have inherent methodologic flaws. We postulate that, if the strength of each approach is appreciated openly and academically, we may come to a combined approach using prescriptive charts that use clinically validated with the use of effective customization. We propose a combined approach by merging datasets on an individual level to test whether variables that are included in customization or the concept of conditional percentiles may be used to determine optimal growth for the individual.
      • Kiserud T.
      • Johnsen S.L.
      Biometric assessment.
      Next, the relationship between these variables and adverse outcomes can and must be explored, although this will remain problematic in retrospective datasets because of treatment paradox. Currently, many retrospective studies compare different strategies in their diagnostic capacity to identify small infants at birth or those infants with adverse outcomes. These comparisons are methodologically flawed because they analyze retrospectively whether these strategies accurately predict birthweight category or adverse outcomes, while ignoring the effects of treatment paradox. Moreover, these comparisons also overlook the issue of the balance of detection rates and false-positive rates that prospective and randomized trials are lacking.
      • Carberry A.E.
      • Gordon A.
      • Bond D.M.
      • Hyett J.
      • Raynes-Greenow C.H.
      • Jeffery H.E.
      Customised versus population-based growth charts as a screening tool for detecting small for gestational age infants in low-risk pregnant women.
      We propose that the combination of the 2 approaches will help achieve the penultimate goal to define normal individual fetal growth patterns. But we should not stop there.

      What we are missing?

      How relevant is fetal size? Size is a consequence of preceding fetal growth that reflects fetal nutrition. Current practice dichotomizes normal and abnormal fetal growth at the 10th percentile. But we need to move beyond “good” or “bad” fetal size. For most continuous measures in human physiologic condition, this is an oversimplification with significant sources of error. First, most fetuses who are identified as small for gestational age are constitutionally small and healthy. Second, many fetuses who have impaired growth and placental dysfunction are of apparent normal weight (Figure 1).
      • Vasak B.
      • Koenen S.V.
      • Koster M.P.
      • et al.
      Human fetal growth is constrained below optimal for perinatal survival.
      Third, fetal size only reflects nutrient transfer function of the placenta and points to the magnitude of placental dysfunction only by association.
      • Baschat A.A.
      Fetal responses to placental insufficiency: an update.
      Stillbirth risk decreases with higher birthweight percentiles, and the majority of fetuses who are born <3rd percentile are known to have been exposed to significant intrauterine hypoxemia. However, there is no percentile above which this risk is excluded (Figure 2).
      • Vasak B.
      • Koenen S.V.
      • Koster M.P.
      • et al.
      Human fetal growth is constrained below optimal for perinatal survival.
      This is further complicated by the poor performance of ultrasound-based fetal growth assessment that detects only up to 50% of babies who are born weighing <10th percentile.
      • Monier I.
      • Blondel B.
      • Ego A.
      • Kaminiski M.
      • Goffinet F.
      • Zeitlin J.
      Poor effectiveness of antenatal detection of fetal growth restriction and consequences for obstetric management and neonatal outcomes: a French national study.
      For the aforementioned reasons, fetal size would be better utilized as a continuous variable in risk calculation.
      Figure thumbnail gr1
      Figure 1Schematic depiction of the overlap and difference between fetal growth restriction and small for gestational age
      The x-axis represents growth percentile; the y-axis represents percentage of the population; the red area represents fetuses with fetal growth restriction.
      AGA, appropriate for gestational age; FGR, fetal growth restriction; LGA, large for gestational age; SGA, small for gestational age.
      Ganzevoort. Fetal growth and risk assessment. Am J Obstet Gynecol 2019.
      Figure thumbnail gr2
      Figure 2Examples of linear relationship between birthweight percentile and clinical outcome
      A, Percentage of 11,576 term fetuses with failure to reach growth potential according to their birthweight percentile group (ie, percentage of fetuses presenting an abnormal cerebroplacental ratio that was calculated after subtraction of those cases with abnormal cerebroplacental ratio in the group with birthweight >90th percentile). From Morales-Rosello J, Khalil A, Morlando M, Papageorghiou A, Bhide A, Thilaganathan B. Changes in fetal Doppler indices as a marker of failure to reach growth potential at term. Ultrasound Obstet Gynecol 2014;43:303-10. With permission. B, Absolute risk per 10,000 pregnancies of term stillbirth by birthweight percentile among 784,576 singleton births in Scottish registries. From Moraitis AA, Wood AM, Fleming M, Smith GC. Birth weight percentile and the risk of term perinatal death. Obstet Gynecol 2014;124:274-83. With permission. C, Perinatal mortality rates according to birthweight percentiles in Dutch Perinatal Registry in all (n=1,170,534) cases at 28–43 weeks gestation, excluding congenital anomalies. From Vasak B, Koenen SV, Koster MP, et al. Human fetal growth is constrained below optimal for perinatal survival. Ultrasound Obstet Gynecol 2015;45:162-7. With permission.
      FRGP, failure to reach growth potential.
      Ganzevoort. Fetal growth and risk assessment. Am J Obstet Gynecol 2019.

      Clinical outcomes of relevance

      The objective of obstetric care is not only to diagnose fetal malnutrition but also to prevent the negative effects of placental dysfunction that include fetal hypoxemia, brain damage, and stillbirth. In postnatal life, protracted nutritional deprivation results in kwashiorkor or marasmus many weeks or months before infant death. In contrast, an infant survives only a very short period with respiratory failure. The placenta is uniquely responsible for many critical body functions, namely nutrition and respiration. To date, clinicians have used fetal size/nutrition as a proxy for placental respiratory failure and risk of stillbirth to avert this risk by timely delivery.
      • Boers K.E.
      • Vijgen S.M.
      • Bijlenga D.
      • et al.
      Induction versus expectant monitoring for intrauterine growth restriction at term: randomised equivalence trial (DIGITAT).
      Many studies evaluate diagnostic tools or interventions by their ability to identify or prevent small babies. The outcomes of relevance, however, should be the variables that indicate fetal hypoxemia (such as stillbirth), the inability to withstand uterine contractions, and long-term neurodevelopmental outcomes.

      A comprehensive approach

      Focusing on fetal size parameters in isolation to detect compromise is a grossly oversimplified diagnostic approach and, as such, is flawed.
      • Poljak B.
      • Agarwal U.
      • Jackson R.
      • Alfirevic Z.
      • Sharp A.
      Diagnostic accuracy of individual antenatal tools for prediction of small-for-gestational age at birth.
      Placental function is reflected across a number of variables that are associated with adverse outcomes that can be examined prenatally.
      • Baschat A.A.
      Fetal responses to placental insufficiency: an update.
      These include Doppler ultrasound scanning of the fetal umbilical, middle cerebral, and maternal uterine arteries, serum biomarkers, and growth trajectory.
      • Gaccioli F.
      • Sovio U.
      • Cook E.
      • Hund M.
      • Charnock-Jones S.
      • Smith G.
      Screening for fetal growth restriction using ultrasound and the sFLT1/PlGF ratio in nulliparous women: a prospective cohort study.
      • Sovio U.
      • Smith G.C.S.
      Blinded ultrasonic fetal biometry at 36 weeks and the risk of emergency caesarean delivery: a prospective cohort study of 3,047 low risk nulliparous women.
      A recent international expert consensus recognized that parameters that indicate placental respiratory function should be included in the assessment.
      • Figueras F.
      • Gratacos E.
      An integrated approach to fetal growth restriction.
      • Gordijn S.J.
      • Beune I.M.
      • Thilaganathan B.
      • et al.
      Consensus definition of fetal growth restriction: a Delphi procedure.
      Currently, these risk factors are used in a categoric fashion, where they have a dose-dependent relationship with poor fetal growth and stillbirth. Risk factors and assessment variables are interdependent, which is a fact that often is disregarded in risk assessment tools that are recommended by national institutions. Finally, stillbirth is a time-dependent outcome rather than an overt disease; as such, it is extremely susceptible to the competing risk and intervention bias of elective delivery.
      It is now possible to use contemporary software tools to generate competing algorithms to undertake comprehensive risk assessment. We propose the development of a predictive approach that takes into account relevant variables in a continuous, nondichotomous manner. Large datasets with longitudinal prospective data currently are generated from on-going clinical intervention trials. We need aggregate individual data from these datasets to allow prediction modelling followed by internal and external validation. Within these algorithms, institutions will be able to choose either type of growth chart (prescriptive or customized) depending on local, regional, or national interpretation. Once individual risk assessment is available, the rational next step is to feed intervention trials.

      Conclusion

      Currently, the 1 issue that dominates much of the debate among valued individual researchers is which growth chart to use to assess normal or abnormal fetal size. We argue that we need to abandon that gridlock because it obscures the bigger and more clinically relevant picture. The current standstill effectively prohibits progress towards the sketched horizon with a comprehensive risk assessment that will benefit the prenatal care for patients.

      References

        • Romero R.
        • Kingdom J.
        • Deter R.
        • Lee W.
        • Vintzileos A.
        Fetal growth: evaluation and management.
        Am J Obstet Gynecol. 2018; 218: S608
        • Crispi F.
        • Miranda J.
        • Gratacos 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-S879
        • 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-S802.e1
        • Caradeux J.
        • Martinez-Portilla R.J.
        • Basuki T.R.
        • Kiserud T.
        • Figueras F.
        Risk of fetal death in growth-restricted fetuses with umbilical and/or ductus venosus absent or reversed end-diastolic velocities before 34 weeks of gestation: a systematic review and meta-analysis.
        Am J Obstet Gynecol. 2018; 218 (S774–82.e21)
        • Lubchenco L.O.
        • Hansman C.
        • Dressler M.
        • Boyd E.
        Intrauterine growth as estimated from liveborn birth-weight data at 24 to 42 weeks of gestation.
        Pediatrics. 1963; 32: 793-800
        • Kloosterman G.J.
        On intrauterine growth - the significance of prenatal care.
        Int J Gynaecol Obstet. 1970; 8: 895-912
        • Visser G.H.
        • Eilers P.H.
        • Elferink-Stinkens P.M.
        • Merkus H.M.
        • Wit J.M.
        New Dutch reference curves for birthweight by gestational age.
        Early Hum Dev. 2009; 85: 737-744
        • Gardosi J.
        • Chang A.
        • Kalyan B.
        • Sahota D.
        • Symonds E.M.
        Customised antenatal growth charts.
        Lancet. 1992; 339: 283-287
        • Gardosi J.
        • Francis A.
        • Turner S.
        • Williams M.
        Customized growth charts: rationale, validation and clinical benefits.
        Am J Obstet Gynecol. 2018; 218: S609-S618
        • Poeran J.
        • Maas A.F.
        • Birnie E.
        • Denktas S.
        • Steegers E.A.
        • Bonsel G.J.
        Social deprivation and adverse perinatal outcomes among Western and non-Western pregnant women in a Dutch urban population.
        Soc Sci Med. 2013; 83: 42-49
        • Lockie E.
        • McCarthy E.
        • Hui L.
        • Churilov L.
        • Walker S.P.
        Feasibility of using self-reported ethnicity in pregnancy according to the gestation related optimal weight classification: a cross-sectional study.
        BJOG. 2018; 125: 704-709
        • De Jong C.L.
        • Gardosi J.
        • Dekker G.A.
        • Colenbrander G.J.
        • Van Geijn H.P.
        Application of a customised birthweight standard in the assessment of perinatal outcome in a high risk population.
        BJOG. 1998; 105: 531-535
        • Gardosi J.
        • Francis A.
        Controlled trial of fundal height measurement plotted on customised antenatal growth charts.
        BJOG. 1999; 106: 309-317
        • Horikoshi M.
        • Beaumont R.N.
        • Day F.R.
        • et al.
        Genome-wide associations for birth weight and correlations with adult disease.
        Nature. 2016; 538: 248-252
        • Verburg B.O.
        • Steegers E.A.
        • De Ridder M.
        • et al.
        New charts for ultrasound dating of pregnancy and assessment of fetal growth: longitudinal data from a population-based cohort study.
        Ultrasound Obstet Gynecol. 2008; 31: 388-396
        • Papageorghiou A.T.
        • Ohuma E.O.
        • Altman D.G.
        • et al.
        International standards for fetal growth based on serial ultrasound measurements: the Fetal Growth Longitudinal Study of the INTERGROWTH-21st Project.
        Lancet. 2014; 384: 869-879
        • Kiserud T.
        • Piaggio G.
        • Carroli G.
        • et al.
        The World Health Organization fetal growth charts: a multinational longitudinal study of ultrasound biometric measurements and estimated fetal weight.
        PLoS Med. 2017; 14: e1002220
        • Kiserud T.
        • Benachi A.
        • Hecher K.
        • et al.
        The World Health Organization fetal growth charts: concept, findings, interpretation, and application.
        Am J Obstet Gynecol. 2018; 218: S619-S629
        • Grantz K.L.
        • Hediger M.L.
        • Liu D.
        • Buck Louis G.M.
        Fetal growth standards: the NICHD fetal growth study approach in context with INTERGROWTH-21st and the World Health Organization Multicentre Growth Reference Study.
        Am J Obstet Gynecol. 2018; 218 (S641–55.e28)
        • Papageorghiou A.T.
        • Kennedy S.H.
        • Salomon L.J.
        • et al.
        The INTERGROWTH-21(st) fetal growth standards: toward the global integration of pregnancy and pediatric care.
        Am J Obstet Gynecol. 2018; 218: S630-S640
        • Francis A.
        • Hugh O.
        • Gardosi J.
        Customized vs INTERGROWTH-21(st) standards for the assessment of birthweight and stillbirth risk at term.
        Am J Obstet Gynecol. 2018; 218: S692-S699
        • Kiserud T.
        • Johnsen S.L.
        Biometric assessment.
        Best Pract Res Clin Obstet Gynaecol. 2009; 23: 819-831
        • Carberry A.E.
        • Gordon A.
        • Bond D.M.
        • Hyett J.
        • Raynes-Greenow C.H.
        • Jeffery H.E.
        Customised versus population-based growth charts as a screening tool for detecting small for gestational age infants in low-risk pregnant women.
        Cochrane Database Syst Rev. 2014; 5: CD008549
        • Vasak B.
        • Koenen S.V.
        • Koster M.P.
        • et al.
        Human fetal growth is constrained below optimal for perinatal survival.
        Ultrasound Obstet Gynecol. 2015; 45: 162-167
        • Baschat A.A.
        Fetal responses to placental insufficiency: an update.
        BJOG. 2004; 111: 1031-1041
        • Monier I.
        • Blondel B.
        • Ego A.
        • Kaminiski M.
        • Goffinet F.
        • Zeitlin J.
        Poor effectiveness of antenatal detection of fetal growth restriction and consequences for obstetric management and neonatal outcomes: a French national study.
        BJOG. 2015; 122: 518-527
        • Boers K.E.
        • Vijgen S.M.
        • Bijlenga D.
        • et al.
        Induction versus expectant monitoring for intrauterine growth restriction at term: randomised equivalence trial (DIGITAT).
        BMJ. 2010; 341: c7087
        • Poljak B.
        • Agarwal U.
        • Jackson R.
        • Alfirevic Z.
        • Sharp A.
        Diagnostic accuracy of individual antenatal tools for prediction of small-for-gestational age at birth.
        Ultrasound Obstet Gynecol. 2017; 49: 493-499
        • Gaccioli F.
        • Sovio U.
        • Cook E.
        • Hund M.
        • Charnock-Jones S.
        • Smith G.
        Screening for fetal growth restriction using ultrasound and the sFLT1/PlGF ratio in nulliparous women: a prospective cohort study.
        Lancet Child Adolesc Health. 2018; 2: 569-581
        • Sovio U.
        • Smith G.C.S.
        Blinded ultrasonic fetal biometry at 36 weeks and the risk of emergency caesarean delivery: a prospective cohort study of 3,047 low risk nulliparous women.
        Ultrasound Obstet Gynecol. 2018; 52: 78-86
        • Figueras F.
        • Gratacos E.
        An integrated approach to fetal growth restriction.
        Best Pract Res Clin Obstet Gynaecol. 2017; 38: 48-58
        • Gordijn S.J.
        • Beune I.M.
        • Thilaganathan B.
        • et al.
        Consensus definition of fetal growth restriction: a Delphi procedure.
        Ultrasound Obstet Gynecol. 2016; 48: 333-339

      Linked Article

      • Counterpoint
        American Journal of Obstetrics & GynecologyVol. 220Issue 1
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          The small for gestational age (SGA; <10th percentile) fetus is at a 7-fold increased risk of dying before delivery.1 Size is an important indicator of fetal growth. Yet, physiologic variation needs to be adjusted for or customized to improve the association with pathologic smallness. The debate about which charts to use needed to be had, and ample evidence has emerged that proves that 1 size does not fit all. An improved standard helps to reassure when smallness is only constitutional and helps to better identify when it is potentially pathologic.
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