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Fetal growth restriction and intra-uterine growth restriction: guidelines for clinical practice from the French College of Gynaecologists and Obstetricians

European Journal of Obstetrics & Gynecology and Reproductive Biology, October 2015, Pages 10 - 18

Abstract

Small for gestational age (SGA) is defined by weight (in utero estimated fetal weight or birth weight) below the 10th percentile (professional consensus). Severe SGA is SGA below the third percentile (professional consensus). Fetal growth restriction (FGR) or intra-uterine growth restriction (IUGR) usually correspond with SGA associated with evidence indicating abnormal growth (with or without abnormal uterine and/or umbilical Doppler): arrest of growth or a shift in its rate measured longitudinally (at least two measurements, 3 weeks apart) (professional consensus). More rarely, they may correspond with inadequate growth, with weight near the 10th percentile without being SGA (LE2).

Birthweight curves are not appropriate for the identification of SGA at early gestational ages because of the disorders associated with preterm delivery. In utero curves represent physiological growth more reliably (LE2). In diagnostic (or reference) ultrasound, the use of growth curves adjusted for maternal height and weight, parity and fetal sex is recommended (professional consensus). In screening, the use of adjusted curves must be assessed in pilot regions to determine the schedule for their subsequent introduction at national level. This choice is based on evidence of feasibility and the absence of any proven benefits for individualized curves for perinatal health in the general population (professional consensus).

Children born with FGR or SGA have a higher risk of minor cognitive deficits, school problems and metabolic syndrome in adulthood. The role of preterm delivery in these complications is linked.

The measurement of fundal height remains relevant to screening after 22 weeks of gestation (Grade C). The biometric ultrasound indicators recommended are: head circumference (HC), abdominal circumference (AC) and femur length (FL) (professional consensus). They allow calculation of estimated fetal weight (EFW), which, with AC, is the most relevant indicator for screening. Hadlock's EFW formula with three indicators (HC, AC and FL) should ideally be used (Grade B). The ultrasound report must specify the percentile of the EFW (Grade C). Verification of the date of conception is essential. It is based on the crown–rump length between 11 and 14 weeks of gestation (Grade A). The HC, AC and FL measurements must be related to the appropriate reference curves (professional consensus); those modelled from College Francais d’Echographie Fetale data are recommended because they are multicentere French curves (professional consensus).

Whether or not a work-up should be performed and its content depend on the context (gestational age, severity of biometric abnormalities, other ultrasound data, parents’ wishes, etc.) (professional consensus). Such a work-up only makes sense if it might modify pregnancy management and, in particular, if it has the potential to reduce perinatal and long-term morbidity and mortality (professional consensus).

The use of umbilical artery Doppler velocimetry is associated with better newborn health status in populations at risk, especially in those with FGR (Grade A). This Doppler examination must be the first-line tool for surveillance of fetuses with SGA and FGR (professional consensus). A course of corticosteroids is recommended for women with an FGR fetus, and for whom delivery before 34 weeks of gestation is envisaged (Grade C). Magnesium sulphate should be prescribed for preterm deliveries before 32–33 weeks of gestation (Grade A). The same management should apply for preterm FGR deliveries (Grade C). In cases of FGR, fetal growth must be monitored at intervals of no less than 2 weeks, and ideally 3 weeks (professional consensus).

Referral to a Level IIb or III maternity ward must be proposed in cases of EFW <1500 g, potential birth before 32–34 weeks of gestation (absent or reversed umbilical end-diastolic flow, abnormal venous Doppler) or a fetal disease associated with any of these (professional consensus). Systematic caesarean deliveries for FGR are not recommended (Grade C). In cases of vaginal delivery, fetal heart rate must be monitored continuously during labour, and any delay before intervention must be faster than in low-risk situations (professional consensus). Regional anaesthesia is preferred in trials of vaginal delivery, as in planned caesareans.

Morbidity and mortality are higher in SGA newborns than in normal-weight newborns of the same gestational age (LE3). The risk of neonatal mortality is two to four times higher in SGA newborns than in non-SGA preterm and full-term infants (LE2). Initial management of an SGA newborn includes combatting hypothermia by maintaining the heat chain (survival blanket), ventilation with a pressure-controlled insufflator, if necessary, and close monitoring of capillary blood glucose (professional consensus).

Testing for antiphospholipids (anticardiolipin, circulating anticoagulant, anti-beta2-GP1) is recommended in women with previous severe FGR (below third percentile) that led to birth before 34 weeks of gestation (professional consensus). It is recommended that aspirin should be prescribed to women with a history of pre-eclampsia before 34 weeks of gestation, and/or FGR below the fifth percentile with a probable vascular origin (professional consensus). Aspirin must be taken in the evening or at least 8 h after awakening (Grade B), before 16 weeks of gestation, at a dose of 100–160 mg/day (Grade A).

Keywords: Small for gestational age, Fetal growth restriction, Adjusted fetal weight curves.

Methods [1], [2], and [3]

The sponsor, the French College of Gynaecologists and Obstetricians, appointed an organization committee (see Appendix A) to define the exact questions to put to a group of expert authors, to choose these experts, follow them up and draft the synthesis of recommendations resulting from their work. The experts analyzed the scientific literature on the subject in order to answer the questions raised. MEDLINE and the Cochrane Library were searched for relevant literature up to mid-2013. The search was restricted to articles published in English and French. Priority was given to articles reporting results of original research, although review articles and commentaries were also consulted. Guidelines of the American College of Obstetricians and Gynecologists [4] and the Royal College of Obstetricians and Gynaecologists [5], a comparison of these two guidelines [6], and guidelines of the World Association of Perinatal Medicine [7] were reviewed, and additional studies were located by reviewing the bibliographies of identified articles.

For each question, each overview of validated scientific date was associated with a level of evidence according to the quality of available data using the working framework defined by the French Health Authority (HAS) as follows.

Quality of evidence assessment

LE1: very powerful randomized comparative trials, meta-analysis of randomized comparative trials.

LE2: not very powerful randomized trials, well-run non-randomized comparative studies, cohort studies.

LE3: case–control studies.

LE4: non-randomized comparative studies with large biases, retrospective studies, transversal studies, series of cases.

A synthesis of recommendations was drafted by the organizing committee based on the replies given by the expert authors. Each recommendation for practice was allocated a level defined by the HAS as follows.

Classification of recommendations

Grade A: recommendations based on good and consistent scientific evidence.

Grade B: recommendations based on limited or inconsistent scientific evidence.

Grade C: recommendations based primarily on consensus and expert opinion.

Professional consensus: in the absence of any conclusive scientific evidence, some practices have nevertheless been recommended on the basis of agreement between the members of the working group (professional consensus).

All texts were reviewed by experts in maternal-fetal medicine who were not involved in the work [i.e. practitioners in the various specialties (see Appendix A) concerned and working in various situations (public, private, university or non-university establishments)]. Following completion of the review process, changes were made, if appropriate, considering assessment of the quality of evidence.

The texts are cited [3], [4], [5], [6], [7], [8], [9], [10], [11], [12], and [13], but the individual references included in each text are not reported here due to space constraints.

Definitions, choice of growth curves [8]

All professionals working with women during the perinatal period are involved in the management of fetal or intra-uterine growth restriction (FGR/IUGR), and must understand the processes involved. All professionals will also benefit from the adoption of a common language based on specific definitions. The clearest possible information must be provided to parents to enable their informed involvement in medical decisions before and after the birth.

The definition of abnormal growth and the choice of a weight curve are the main determinants of screening for, and diagnosis of, FGR.

Definitions

The following terminology is proposed for use both before and after birth.

  • Small for gestational age (SGA) (used most often as an adjective, to be read as small size for gestational age when used as a noun) is defined by weight (in utero estimated weight or birth weight) below the 10th percentile (professional consensus). Severe SGA is SGA below the third percentile (professional consensus).
  • FGR/IUGR usually corresponds with SGA associated with evidence indicating abnormal growth (with or without abnormal uterine and/or umbilical Doppler): arrest of growth or a shift in its rate measured longitudinally (at least two measurements, 3 weeks apart) (professional consensus). More rarely, FGR/IUGR may correspond with inadequate growth, with weight near the 10th percentile without being SGA (LE2). IUGR is appropriate when there is evidence that a fetus, placenta and amniotic fluid are all growth restricted; however, when (as is usually the case) the diagnosis is based on birth weight, FGR is more appropriate.

Comments

  • When SGA is diagnosed based on a single measurement, the existence of signs of impaired fetal well-being (reduced fetal movement, Doppler abnormalities, oligohydramnios) must suggest FGR (professional consensus).
  • SGA children are either constitutionally small or authentically growth restricted (LE2).
  • Terms such as ‘hypotrophic’ or ‘symmetrically or asymmetrically growth restricted’ should be removed from the medical vocabulary (professional consensus).

Choice of curves

  • Birthweight curves are not appropriate for the identification of SGA at early gestational ages because of the disorders associated with preterm delivery. In utero curves represent physiological growth more reliably (LE2).
  • Fetal sex, maternal height and weight at the beginning of pregnancy, parity and ethnic origin influence fetal weight significantly; fetal sex is the predominant factor (LE2). The use of a curve undifferentiated by sex leads to the preferential suspicion of SGA in girls (false positives) and to ignoring SGA in boys (false negatives) (LE3).
  • Individual adjusted curves of fetal growth combine in utero growth and adjustment for maternal height and weight, parity and fetal sex. SGA defined solely according to a curve in the general population does not present an increased perinatal risk, and seems simply to indicate that the infant is constitutionally small. SGA babies defined solely according to individual adjusted fetal weight curves have an excess risk of perinatal death of 2–10% (LE3). Overall, 5% of all children are reclassified, including 25% of SGA babies (LE3).
  • Overall, the homogeneous adoption of new growth curves for prenatal and postnatal periods is necessary for all professionals involved in perinatal care (obstetricians, midwives, ultrasonographers, paediatricians, etc.) (professional consensus).
  • In diagnostic (or reference) ultrasound, the use of growth curves adjusted for maternal height and weight, parity and fetal sex is recommended (professional consensus).
  • In screening, the use of adjusted curves must be assessed in pilot regions to determine the schedule for their subsequent introduction at national level. This choice is based on evidence of feasibility, and the absence of any proven benefits for individualized curves for perinatal health in the general population (professional consensus).

Risk factors for SGA [9]

  • A history of SGA increases the risk of another SGA child four-fold (LE2).
  • Maternal age >35 years triples the risk of SGA compared with women aged 20–30 years (LE2).
  • Primiparity and grand multiparity double the risk of SGA (LE2–3).
  • Hypertensive disorders increase the frequency of SGA: chronic hypertension (by a factor of 2), pre-eclampsia (by a factor of 5–12, varying by severity and by study) and pregnancy-related hypertension (by a factor of 2) (LE2).
  • Pre-existing diabetes before pregnancy with vascular damage is associated with SGA (risk multiplied by 6) (LE3).
  • Smoking 10 cigarettes/day during pregnancy doubles the risk of SGA, with a dose–effect relationship (LE2).
  • Drinking alcohol also doubles the risk of SGA (LE2).
  • Use of illegal drugs during pregnancy triples the risk of SGA (LE2).
  • Other risk factors, including underweight, obesity and disadvantaged socio-economic status, increase the risk of SGA by a factor of less than 2 (LE2).

Long-term consequences for children born SGA or FHR [10]

The principal difficulty in determining these consequences lies in dissociating the intermediate and long-term effects of FGR or SGA from the effects due to preterm birth.

  • Neurodevelopmental scores at 2 years of age are lower in these children, whether born preterm or at term, and the effect is more marked in FGR children compared with SGA children (LE3).
  • Recent interventional studies regarding the time and type of delivery in this population have not succeeded in identifying effects on development at 2 years or at 6–13 years of age (LE2).
  • As with normal-sized children, the mother's wish to breast feed must be supported. Development appears best in these children when they are breast fed, despite their poorer weight/height growth curve (‘breastfeeding paradox’) (LE3).
  • SGA/FGR children have a higher risk of minor cognitive deficiencies, symptoms of hyperactivity and attention deficit at 5 years of age, and a higher risk of school problems at 8 years of age (LE3). In children born before 28 weeks of gestation, the effects due to prematurity are more marked than those due to growth restriction (LE3).
  • SGA/FGR children are at higher risk of cardiovascular diseases, hypertension, glucose intolerance, diabetes, dyslipidaemia and obesity in adulthood (LE2).
  • Most SGA/FGR children have caught up in weight and height by 6 months and 1 year, respectively (LE3). Catch-up growth (both height and weight) that is too rapid may be a supplementary factor in the onset of hypertension (LE2).
  • Studies of adults born SGA have not shown repercussions in terms of quality of life, employability or self-esteem (LE3).
  • In conclusion, FGR or SGA children have a higher risk of minor cognitive deficits, school problems and metabolic syndrome in adulthood. The role of preterm delivery in these complications is linked.

Modalities of screening and diagnosis of SGA fetuses [11]

The performance of ultrasound for screening for SGA is low in France, with a sensitivity of 22%.

Clinical screening

  • The measurement of fundal height remains relevant to screening after 22 weeks of gestation (Grade C).
  • This measurement can help screen for SGA because a growth defect may appear between the 22- and 32-week ultrasounds, or after 32 weeks of gestation (Grade C). An abnormal fundal height justifies a supplementary ultrasound (professional consensus).

Ultrasound screening

  • Fetal biometry must be interpreted according to the clinical and ultrasound context (Grade C).
  • The biometric ultrasound indicators defined by the Ultrasound Advisory Committee are recommended: head circumference (HC), abdominal circumference (AC) and femur length (FL) (professional consensus).
  • HC, AC and FL measurements enable calculation of estimated fetal weight (EFW), which, together with AC, is the most relevant indicator for screening. Hadlock's EFW formula with three indicators (HC, AC and FL) should ideally be used (Grade B). EFW has demonstrated its usefulness in populations at high and low risk of SGA. For 95% of women, EFW has a maximum error of ±20%. This means that the difference between EFW and real fetal weight exceeds 20% for 5% of women (LE2).
  • EFW is used for screening in order to improve performance and to make practices more consistent (and results more comparable) (Grade C).
  • EFW has the advantage of sharing a common language with paediatricians and facilitating communication with parents (provided that it is clearly stated that it is only an estimate and the margins of error are mentioned).
  • The ultrasound report must specify the percentile of the EFW (Grade C).
  • It should be borne in mind that a fetus whose biometric measurements are all at or above the 10th percentile can still have an EFW below the 10th percentile.
  • Verification of the date of conception is essential. This is based on the crown–rump length between 11 and 14 weeks of gestation (Grade A).
  • HC, AC and FL measurements must be related to the appropriate reference curves (professional consensus). From 18 to 41 weeks of gestation, the curves recommended are those modelled from Collège Français d’échographie Fœtale data because these are multicentre French curves (professional consensus).
  • Professional practice evaluation of the techniques and distribution of measurements of ultrasound indicators must be encouraged (professional consensus).
  • A routine supplementary ultrasound at the end of pregnancy (in additon to the third-trimester ultrasound) is not necessary (Grade A), except when clinical evidence indicates a need (Grade C).
  • In a population at low risk of SGA and in the framework of ultrasound screening, a referral must be offered when the EFW is below the third percentile, even in the absence of any other clinical or ultrasound anomaly. In this case, specificity is favoured over sensitivity (professional consensus).
  • For populations at risk of SGA or when a clinical or ultrasound (including Doppler) anomaly is present, the threshold of the 10th percentile is chosen for referrals. In this case, sensitivity is favoured over specificity (professional consensus).
  • An expert opinion is also recommended for a non-SGA fetus with inadequate growth between two examinations (e.g. no change in EFW over a 3-week period) (professional consensus).
  • After 24 weeks of gestation, management is more urgent because of fetal viability.
  • If the biometric examination must be repeated to help diagnose FGR, the minimum interval is 3 weeks (Grade B). This interval can be shorter if the EFW has an important role in the decision for possible medically indicated early delivery (professional consensus).

Causal work-up for FGR [12]

  • Whether or not a work-up should be performed and its content depend on the context (term, severity of biometric abnormalities, other ultrasound data, parents’ wishes, etc.) (professional consensus).
  • Such a work-up only makes sense if it might modify pregnancy management and, in particular, if it has the potential to reduce perinatal and long-term morbidity and mortality (professional consensus).
  • These additional investigations have two principal objectives: to assess fetal vitality and the possibilities for continuing the pregnancy in conditions that are safe for both mother and fetus; and to determine the cause of SGA. This work-up should be envisaged when the EFW is below the 10th percentile or below the fifth percentile (or at least when the abdominal circumference is below the 10th percentile) (professional consensus).
  • Coordination and homogenization of practices within care networks are recommended, working with the prenatal diagnostic centre (professional consensus).
  • Management (and, where appropriate, the work-up) must be performed on an emergency basis in the case of maternal vascular symptoms or a Doppler umbilical artery velocimetry anomaly such as absent diastole or reverse flow (professional consensus).
  • The work-up must review the principal items in the history and clinical findings (professional consensus).
  • An ultrasound will be performed to confirm and specify the biometric abnormalities and to search for other abnormalities of the fetus, amniotic fluid, placenta and Doppler results.
  • Screening for maternal–fetal cytomegalovirus infections by a simple maternal serology test can be offered at the outset in the absence of evidence of a vascular cause.
  • The principal difficulty is deciding whether invasive sampling (usually amniocentesis) must be performed. This sample will undergo, depending on the case, assessment for infection, chromosomal and/or gene analysis, or other more specific assays.
  • Amniocentesis is not indicated routinely for a work-up for SGA or FGR, and must be discussed with the prenatal diagnostic centre.
  • In practice, the principal factors suggesting that invasive sampling would be useful are:
  • early and/or severe biometric anomaly;
  • association with an excessive quantity of amniotic fluid;
  • association with one or more morphological anomalies;
  • absence of a Doppler abnormality;
  • absence of another evident cause;
  • parental desire for a prenatal diagnosis; and
  • results that might modify the management.

Prenatal surveillance and indications for delivery in cases of isolated vascular FGR [13]

Prenatal surveillance

The modalities of fetal surveillance must be appropriate for the severity of FGR, the gestational age and the Doppler findings (professional consensus).

Available surveillance tools

  • Umbilical artery Doppler velocimetry and fetal cardiotocography are the first-line surveillance tools to be implemented in cases with a diagnosis of FGR (professional consensus).
  • Conventional FHR, despite the strong interobserver variability in its analysis, remains an essential element in surveillance of SGA/FGR fetuses (professional consensus).
  • At present, there is insufficient evidence to recommend for or against routine surveillance of short-term variability, even before 32 weeks of gestation (Grade C). Nonetheless, in view of its objective and reproducible nature, short-term variability can provide decision support about the need to deliver FGR infants before 32 weeks of gestation (professional consensus).
  • The use of umbilical artery Doppler velocimetry is associated with better newborn health status in populations at risk, and especially in those with FGR (Grade A). This Doppler examination must be the first-line tool for surveillance of fetuses with SGA and FGR (professional consensus).
  • Despite the absence of randomized trials to demonstrate potential clinical benefits, the high predictive value of a cerebral Doppler examination, compared with examination of the umbilical artery alone, makes it possible to offer it routinely for fetuses with suspected FGR, regardless of whether or not the umbilical artery Doppler is normal (Grade C).
  • Pregnancies with FGR fetuses do not always follow the standard sequence, in which deterioration occurs first in the arterial Doppler index, then the venous Doppler index and finally in the cardiotocographic tracing.
  • The venous Doppler must only be performed by trained operators and only in pregnancies with FGR in which delivery before 32 weeks of gestation is envisaged (Grade C).

Modalities of surveillance and management

  • Hospitalization is not indicated routinely for surveillance of fetuses with SGA/FGR. This decision depends on the organization of care at each facility (Grade C).
  • A course of corticosteroids is recommended for patients with FGR fetuses and for whom delivery before 34 weeks of gestation is envisaged (Grade C).
  • Magnesium sulphate should be prescribed for preterm deliveries before 32–33 weeks of gestation (Grade A). There is no evidence to justify a different attitude for preterm FGR deliveries (Grade C). This administration should ideally take place in the hours before the birth.
  • In cases of FGR, fetal growth must be monitored at intervals of no less than 2 weeks, and ideally 3 weeks (professional consensus).
  • If the Doppler umbilical artery velocimetry shows normal diastole, it should be repeated every 2–3 weeks and combined with a cerebral artery Doppler and biometric measurements. The frequency of this surveillance should be adjusted to the severity of FGR (professional consensus).
  • If the umbilical artery Doppler velocimetry is abnormal but diastole is still positive, and if early delivery is not envisaged, surveillance by umbilical and cerebral artery Doppler velocimetry and FHR should be repeated weekly or more often, depending on the severity of FGR. For cerebral artery Doppler, a cerebroplacental Doppler ratio <1 or below the fifth percentile is considered routinely for management. This surveillance can be performed on an outpatient basis (professional consensus).
  • In the case of absent diastole or reverse flow on the umbilical artery Doppler velocimetry, hospitalization must be considered to administer a course of corticosteroids and organize surveillance, or even delivery. FHR should then be performed daily (professional consensus).

Indications for immediate delivery

  • Induced preterm delivery has major consequences that justify conservative treatment even in cases with abnormal umbilical artery Dopplers (Grade B).
  • Isolated arrested fetal growth (with normal fetal Doppler results and normal FHR) is not, in itself, an indication for immediate delivery (professional consensus).
  • A pulsatility index of the ductus venosus above the 95th percentile and FHR abnormalities (short-term variability <3 ms or rhythm with little oscillation or repeated decelerations) are independent criteria for delivery of infants with FGR <32 weeks of gestation. Delivery must be envisaged when either of these two indicators is persistently abnormal (professional consensus).
  • The two possible options are delivery or expectant management (Grade B).
  • In cases of reverse flow or permanent absent diastole on the umbilical artery Doppler velocimetry after 34 weeks of gestation, delivery should be envisaged (Grade C).
  • In the case of abnormal umbilical artery Doppler velocimetry with positive diastolic flow, enhanced surveillance should include umbilical and cerebral artery Doppler velocimetry and FHR several times a week. Surveillance on an outpatient basis is possible (professional consensus).
  • Birth can be envisaged from 37 weeks of gestation, based on the EFW, quantity of amniotic fluid and Doppler measurements. The route of delivery will take maternal and obstetric characteristics (parity, previous caesarean, body mass index, local cervical condition) into account (Grade C).
gr1

Fig. 1 Management of fetal growth restriction before 32 weeks of gestation without absent or reversed end-diastolic flow in the umbilical artery. UAD, umbilical artery doppler; EFW, estimated fetal weight; AFI, amniotic fluid index; CAD, cerebral artery Doppler; FHR, fetal heart rate; STV, short-term variability.

gr2

Fig. 2 Management of fetal growth restriction before 32 weeks of gestation with absent or reversed end-diastolic (ARED) flow in the umbilical artery. EFW, estimated fetal weight; AFI, amniotic fluid index; UAD, umbilical artery Doppler; CAD, cerebral artery Doppler; FHR, fetal heart rate; STV, short-term variability; DV, ductus venosus.

Role of termination of pregnancy and palliative care in cases of fetal or intra-uterine vascular growth restriction [14]

Two circumstances can raise the question of termination of pregnancy in vascular FGR:

  • when fetal prognosis appears so compromised that the newborn's chances of survival in good conditions appear very low; and
  • when the mother's life is endangered, most often because of pre-eclampsia.

Gestational age and weight are two major prognostic criteria (LE1).

  • The prognostic assessment is based essentially on ultrasound, which must be performed by a senior physician. EFW, growth rate, fetal Doppler findings and signs of chronic hypoxia (e.g. hyperechoic intestines, oligohydramnios) must all be considered (professional consensus).
  • An interval of at least 2 weeks (ideally 3 weeks) should elapse between two examinations to minimize the error associated with the imprecision of EFW (professional consensus).
  • In some cases, in utero death can occur during this interval necessary for diagnosis and prognosis; this risk must be explained to the parents (professional consensus).
  • Collaboration between the obstetrician and paediatrician is essential, and they should jointly provide the parents with information (professional consensus).

When the fetal prognosis appears reserved, several approaches can be considered with the parents.

  • They may move towards an expectant approach, aware that death in utero may occur, in a time period that is difficult to predict (professional consensus).
  • The couple may also prefer active management with immediate delivery, postnatal assessment and the possibility of secondary development towards support with palliative care (professional consensus). It nonetheless exposes the mother to both the short- and long-term morbidity associated with a caesarean that most often involves incision into the uterine body.
  • Finally, the couple may choose to request a medically indicated termination of pregnancy. In such a case, the request must be presented to a multidisciplinary prenatal diagnosis centre, regardless of whether the indication is fetal or maternal. Exemption from this regulatory obligation is only possible in maternal emergencies (and then the exemption is only to the advance request for authorization).
  • Regardless of the couple's decision, they must receive support. Psychological support must be offered to them both before and after the birth (professional consensus).

Modalities of birth of fetuses with FGR [15]

Interventions and place of birth of fetuses with FGR

  • The diagnosis of a fetus with FGR justifies referral to an appropriate maternity ward able to provide obstetric, neonatal and possibly maternal management, in compliance with the regional perinatal care network protocols (professional consensus).
  • Referral to a Level IIb or III maternity ward must be proposed in cases of EFW <1500 g, potential birth before 32–34 weeks of gestation (absent umbilical flow diastolic end flow or reverse flow, Doppler venous anomaly) or a fetal disease associated with any of these (professional consensus).

Route of delivery of SGA/FGR fetuses

  • Systematic caesarean deliveries for FGR are not recommended (Grade C).
  • In cases of vaginal delivery, fetal heart rate must be recorded continuously during labour, and any delay before intervention must be faster than in low-risk situations (professional consensus).
  • Caesareans are habitual at early term or in cases of severe abnormalities of the umbilical artery Doppler velocimetry (absent diastolic index or reverse flow), although no data are available about trial of vaginal delivery in favourable situations (ripened permeable cervix, multiparity, cephalic presentation) (professional consensus).
  • There is no evidence to contraindicate induction of labour for FGR, even before term and/or with an unripe cervix (Grade C).
  • When the cervix is not ripe, intracervical or intravaginal prostaglandins or an intracervical balloon can be used, except in very-high-risk situations (very early term and/or reverse flow on the umbilical artery Doppler) (professional consensus).
  • After placement of the prostaglandins or of an intracervical balloon, surveillance must continue beyond the first 2 h (professional consensus).
  • Use of an oxytocin test before induction for FGR is not recommended (professional consensus).
  • Neither a routine instrumental intervention nor a systematic episiotomy is recommended (professional consensus).

Breech presentation

  • There is no evidence in the literature to contraindicate vaginal delivery for a woman in labour with a fetus with FGR in breech presentation (professional consensus).
  • Vaginal delivery must be assessed according to the extent of FGR and the obstetric conditions (professional consensus).

Mode of anaesthesia during labour and in caesarean deliveries

  • Regional anaesthesia is preferred in trials of vaginal delivery, as in planned caesareans.
  • In caesareans under spinal anaesthesia, adequate anaesthetic management must endeavour to maintain blood pressure at its normal value. It appears desirable to shorten the delay between induction of anaesthesia and actual fetal delivery (the obstetrician should be available immediately) (Grade B).

Management of SGA newborns and early outcome [16]

The principal early complications of SGA differ notably from those for term newborns and preterm newborns who are not SGA.

Assessment of the cause

  • The investigation always includes a clinical examination with an HC measurement. Additional investigations depend on those already performed during the prenatal period and on the likelihood of a non-vascular disease (professional consensus).

Complications associated with low birth weight

  • Morbidity and mortality are higher in SGA newborns than in normal-weight newborns of the same gestational age (LE3).
  • The risk of neonatal mortality is two to four times higher in SGA newborns than in non-SGA preterm and full-term infants (LE2).
  • The risks are simultaneous for perinatal (especially perinatal anoxia-ischaemia in term newborns), early postnatal (particularly hypothermia and hypoglycaemia) and later consequences (e.g. bronchopulmonary dysplasia, pulmonary hypertension and enteropathy in preterm SGA newborns).
  • The risk of hyaline membrane disease is not significantly higher in SGA than non-SGA newborns (LE2).
  • From the neurological perspective, periventricular leukomalacia is not more frequent, but the results for severe intraventricular haemorrhage and retinopathy of prematurity are controversial (expert opinion).
  • The increased risk of poor adaptation to extra-uterine life in SGA newborns must be anticipated by a paediatric consultation before birth for infants with severe SGA (below third percentile), given that that fetal weight is estimated and thus subject to inherent margins of error (professional consensus).
  • Initial management of an SGA newborn includes combatting hypothermia by maintaining the heat chain (survival blanket), ventilation with a pressure-controlled insufflator, if necessary, and close monitoring of capillary blood glucose (professional consensus).
  • Transfer to a special unit, especially in a different facility, depends on the infant's weight and adaptation to extra-uterine life; promoting proximity between mother and child remains important (professional consensus).

Pathological examination of the placenta [17]

  • A pathological examination of the placenta should be performed in the case of FGR or IUGR at or below the third percentile (professional consensus).
  • The request form for examination of the placenta must include information about the pregnancy, delivery and child. A standard information form accompanying the request facilitates the transmission of these data (professional consensus).
  • The most common placental lesions in IUGR are those compatible with placental vascular insufficiency of maternal origin:
  • infarction;
  • decidual arterial disease;
  • syncytial clusters; and
  • villous chorangiosis.
  • These lesions are variable, non-specific and most suggestive when they are found together (expert opinion).
  • There are other placental diseases that can cause IUGR, including abnormalities of the configuration of the placenta, cord abnormalities and diseases of the placental parenchyma, which must be diagnosed microscopically (expert opinion).
  • This is particularly the case for fetal thrombotic vasculopathy, chronic villitis and chronic histiocytic intervillositis. These can recur and have notable clinical implications for mother and child (expert opinion).

Prevention of FGR [18]

Before a first pregnancy

Due to the risk factors for FGR, it is recommended:

  • to encourage women planning to become pregnant to aim to reach a preconceptional body mass index <30 kg/m2 and >18 kg/m2 (professional consensus);
  • to encourage them to stop smoking (Grade A) and offer them assistance in doing so (professional consensus). The same is true for alcohol and drugs (professional consensus); and
  • to limit multiple pregnancy in cases of assisted reproductive technology (Grade A).

Among women at increased risk of FGR

  • Some chronic maternal diseases (diabetes, lupus and chronic hypertension) are associated with an increased risk of FGR, especially for women with kidney damage (LE4).
  • A multidisciplinary consultation before conception is particularly indicated to assess these risks, adjust treatments to the attempt to become pregnant, and plan the pregnancy for the best moment of the disease (professional consensus).

During pregnancy, to avoid the onset of FGR

In cases without chronic maternal disease
  • It is recommended to comply with the weight objectives recommended by the Institute of Medicine as a function of preconceptional body mass index (Grade B).
  • Women must be encouraged to stop smoking and consuming any other toxic substances as early as possible in the pregnancy (professional consensus).
  • There is no evidence to support recommending rest for prevention of FGR (professional consensus).
  • Routine iron supplementation does not reduce the risk of FGR (LE1).
In cases of chronic maternal disease
  • For diabetes that preceded pregnancy, it is recommended that glycaemic objectives should be maintained in avoiding hypoglycaemia (Grade B).
  • For chronic hypertension, it is recommended that systolic blood pressure should be maintained between 140 and 160 mmHg, and diastolic blood pressure should be maintained between 90 and 110 mmHg; this can require that treatment for hypertension be stopped during the pregnancy (professional consensus).

For pregnant women with a history of FGR

  • It is recommended to test for antiphospholipids (anticardiolipin, circulating anticoagulant, anti-beta-GP1) in women with previous severe FGR (below third percentile) that led to birth before 34 weeks of gestation (professional consensus).
  • There is no evidence to support testing for other thrombophilias in women with a history of FGR (professional consensus).
  • An interval of 18–23 months between two pregnancies seems to be associated with a lower rate of FGR (expert opinion).

Role of aspirin

  • It is recommended that aspirin should be prescribed to women with a history of pre-eclampsia before 34 weeks of gestation and/or FGR below the fifth percentile with a probable vascular origin (professional consensus).
  • Aspirin must be taken in the evening or at least 8 h after awakening (Grade B), before 16 weeks, at a dose of 100–160 mg/day (Grade A).
  • Some diseases are associated with a increased risk of vascular FGR; nonetheless, there is no evidence in the literature on which to base a recommendation for prescribing aspirin in these situations (professional consensus): chronic hypertension, pregestational diabetes, lupus, chronic nephropathy and sickle cell anaemia.

Condensation

Guidelines for clinical practice from the French College of Gynaecologists and Obstetricians on fetal growth restriction/intra-uterine growth restriction.

A.1. Steering committee

B. CARBONNE, President (gynaecologist/obstetrician, Hôpital Trousseau, Paris, France), C. VAYSSIERE, Coordinator (gynaecologist/obstetrician, CHU Toulouse, Toulouse, France), L. SENTILHES, Coordinator (gynaecologist/obstetrician, CHU Angers, Angers, France), C. ARNAUD, Methodologist (epidemiologist, INSERM U1027, Toulouse, France), D. COMBOURIEU (Collège Français d’échographie Fœtale, Lyon, France), V. TESSIER (midwife, CNSF, CHU Bicêtre, Le Kremlin-Bicêtre, France), B. LANGER (gynaecologist/obstetrician, Société Française de Médecine Périnatale, CHU Hautepierre, Strasbourg, France), P. TRUFFERT (neonatologist, Société Française de Néonatologie, CHRU Lille, France), A. SERRY (Collectif Interassociatif Autour de la Naissance, Paris, France) and C. BERNARD (Collectif Interassociatif Autour de la Naissance, Paris, France).

A.2. Working group

A. EGO (epidemiologist, INSERM U953, CHU Grenoble, Grenoble, Paris), C. FLAMANT (paediatrician, CHU Nantes, Nantes, France), A. GAUDINEAU (gynaecologist/obstetrician CHU Strasbourg, Strasbourg, France) G. GASCOIN (paediatrician, CHU Angers, Angers, France), G. GRANGÉ (gynaecologist/obstetrician, CHU Cochin, Paris France), V. HOUFFLIN-DEBARGE (gynaecologist/obstetrician, CHRU Jeanne de Flandre, Lille, France), V. MALAN (genetician, CHU Necker, Paris, France), P. MARCORELLES (anatomopathologist, CHU Brest, Brest, France), J. NIZARD (gynaecologist/obstetrician, CHU Pitié, Paris, France), F. PERROTIN (gynaecologist/obstetrician, CHU Tours, Tours, Paris), L. SALOMON (gynaecologist/obstetrician, CHU Necker, Paris, France), M.V. SENAT (gynaecologist/obstetrician, CHU Bicêtre, Le Kremlin-Bicêtre, Paris) and V. TSATSARIS (gynaecologist/obstetrician, CHU Cochin, Paris).

A.3. Peer reviewers

E. AZRIA (gynaecologist/obstetricia, CHU Bichat, Paris, France), M. BECHARD DE SPIRLET (gynaecologist/obstetrician, Levallois-Perret, France), C. BLANCHOT-ISOLA (midwife, Evry, France), B. BRANGER (paediatrician, CHU Nantes, France), (gynaecologist/obstetrician, CH Cholet, Cholet, France), H. BRUEL (paediatrician, CHG, Montivilliers, France), A. BURGUET (paediatrician, CHU Dijon, Dijon, France), D. CARLES (fetopathologist, CHU Bordeaux, Bordeaux, France), M.L. CHARKALUK-DUPONT (paediatrician, Lille, France), F. COATLEVEN (gynaecologist/obstetrician, CHU Bordeaux, Bordeaux, France), P. DAUNE (midwife, CHU Amiens, Amiens, France), I. de MEZERAC (Association SPAMA, Soins Palliatifs et Accompagnement en Maternité, Lille, France), M. DREYFUS (gynaecologist/obstetrician, CHU Caen, Caen, France), M. DRIESSEN (gynaecologist/obstetrician, CHU, Paris), G. DUCARME (gynaecologist/obstetrician, CH La Roche sur Yon, La Roche sur Yon, France), C. FOULHY (midwife, CHU Clermond-ferrand, Clermond-Ferrand, France), D. GALLOT (gynaecologist/obstetrician, CHU Clermont-Ferrand, Clermont Ferrand, France), F. GOFFINET (gynaecologist/obstetrician, CHU Cochin, INSERM U953, Paris, France), S. GONY (midwife, CHU Clermont Ferrand, Clermont Ferrand, France), I. GUELLEC (paediatrician, CHU Trousseau, Paris, France), T. HARVEY (gynaecologist/obstetrician, Hôpital Diaconesses, Paris, France), J.M. JOUANNIC (gynaecologist/obstetrician, CHU Trousseau, Paris, France), O. JOURDAIN (gynaecologist/obstetrician, Bruges, Belgique), G. KAYEM (gynaecologist/obstetrician, CHU Louis Mourier, Colombes, France), R. KUTNAHORSY (gynaecologist/obstetrician, CH Colmar, Colmar, France), H. LAURICHESSE (gynaecologist/obstetrician, CHU Clermont-Ferrand, Clermont-Ferrand, France), A. LEREBOURS-BARBIER (gynaecologist/obstetrician, Vannes, France), M. MARTINEZ (midewife, CHU Montpellier, Montpellier, France), E. MASCITTI-HUMBERT (midwife, CH Chaumont, Chaumont, France), C. MORIN (midewife, CHU Bordeaux, Bordeaux, France), M. MORIN (midwife, CHU Toulouse, Toulouse, France), I. NISAND (gynaecologist/obstetrician, CHU Hautepierre, Strasbourg, France), M. PERINEAU (gynaecologist/obstetrician, Clinique Sarrus-Teinturiers, Toulouse, France), A. RICBOURG (gynaecologist/obstetrician, CHU Lariboisière, Paris, France), V. RIGOURD (paediatrician, Paris, France), C. ROUILLARD (midwife, CHU Angers, Angers, France), P. ROZENBERG (gynaecologist/obstetrician, CHI Poissy, Poissy, France), B. SCHAUB (gynaecologist/obstetrician, CHU, de Fort de France, Fort de France, France), J. SEROR (sonographist, Paris, France), O. THIEBAUGEORGES (gynaecologist/obstetrician, Clinique Sarrus-Teinturiers, Toulouse, France), E. VERSPYCK (gynaecologist/obstetrician, CHU Rouen, Rouen, France), J. ZEITLIN (epidemiologist, INSERM U953, Paris, France).

References

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  • [3] B. Carbonne, L. Sentilhes, C. Vayssière. Intrauterine growth retardation: guidelines for clinical practice: introduction. J Gynecol Obstet Biol Reprod. 2013;42:868-869 Crossref
  • [4] American College of Obstetricians and Gynecologists. Intrauterine growth restriction. (ACOG, Washington, DC, 2000)
  • [5] Royal College of Obstetricians and Gynecologists. The investigation and management of the small-for-gestational-age fetus. Guideline No. 31. (RCOG, London, 2002)
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Footnotes

a Service de Gynécologie-Obstétrique, CHU Toulouse Hôpital Paule de Viguier, Toulouse, France

b INSERM UMR1027, Université Toulouse III, Toulouse, France

c Service de Gynécologie-Obstétrique, CHU Angers, Angers, France

d Université Grenoble Alpes, TIMC-IMAG, Grenoble, France

e CNRS, TIMC-IMAG, Grenoble, France

f CHU Grenoble, Pôle Santé Publique, Grenoble, France

g Collectif Interassociatif Autour de la Naissance, Paris, France

h Cabinet médical, Lyon, France

i Service de réanimation et médecine néonatales, hôpital mère-enfant, CHU de Nantes, Nantes, France

j Service de réanimation et médecine néonatales, pôle femme-mère-enfant, CHU d’Angers, Angers, France

k Département de gynécologie-obstétrique, hôpitaux universitaires de Strasbourg, Strasbourg, France

l Maternité Port-Royal, groupe hospitalier Cochin – hôtel-Dieu, Paris, France

m Clinique d’obstétrique, pôle femme – mère-nouveau-né, hôpital Jeanne-de-Flandre, CHRU de Lille, Lille, France

n Cytogénétique, hôpital universitaire Necker-Enfants-Malades, Paris, France

o Service d’anatomie pathologique, pôle biologie pathologie, hôpital Morvan, CHRU de Brest, Brest, France

p Service de gynécologie obstétrique, CHU Pitié-Salpêtrière, Paris, France

q Pôle de gynécologie obstétrique, médecine fœtale, médecine et biologie de la reproduction, centre Olympe de Gouges, CHRU de Tours, Tours, France

r Maternité, hôpital universitaire Necker-Enfants-Malades, Paris, France

s Service de gynécologie-obstétrique, hôpital Bicêtre, Le Kremlin-Bicêtre, France

t Service de réanimation néonatale, hôpital Jeanne-de-Flandre, CHRU de Lille, Lille, France

u Unité d’obstétrique – maternité, hôpital Trousseau, Assistance Publique – Hôpitaux de Paris, université Pierre-et-Marie-Curie-Paris 6, France

Corresponding author at: Hôpital Paule de Viguier, CHU Toulouse, 330 av de Grande Bretagne, 31059 Toulouse, France. Tel.: +33 567771216; fax: +33 567771219.