European Journal of Obstetrics & Gynecology and Reproductive Biology 193 (2015) 1018

Contents lists available at ScienceDirect

European Journal of Obstetrics & Gynecology and

Reproductive Biology
journal homepage: www.elsevier.com/locate/ejogrb

Fetal growth restriction and intra-uterine growth restriction:

guidelines for clinical practice from the French College of
Gynaecologists and Obstetricians
C. Vayssie`re a,b,*, L. Sentilhes c, A. Ego d,e,f, C. Bernard g, D. Cambourieu h, C. Flamant i,
G. Gascoin j, A. Gaudineau k, G. Grange l, V. Houfin-Debarge m, B. Langer k, V. Malan n,
P. Marcorelles o, J. Nizard p, F. Perrotin q, L. Salomon r, M.-V. Senat s, A. Serry g, V. Tessier s,
P. Truffert t, V. Tsatsaris l, C. Arnaud b, B. Carbonne u
a
Service de Gynecologie-Obstetrique, CHU Toulouse Hopital Paule de Viguier, Toulouse, France
b
INSERM UMR1027, Universite Toulouse III, Toulouse, France
c
Service de Gynecologie-Obstetrique, CHU Angers, Angers, France
d
Universite Grenoble Alpes, TIMC-IMAG, Grenoble, France
e
CNRS, TIMC-IMAG, Grenoble, France
f
CHU Grenoble, Pole Sante Publique, Grenoble, France
g
Collectif Interassociatif Autour de la Naissance, Paris, France
h
Cabinet medical, Lyon, France
i
Service de reanimation et medecine neonatales, hopital me`re-enfant, CHU de Nantes, Nantes, France
j
Service de reanimation et medecine neonatales, pole femme-me`re-enfant, CHU dAngers, Angers, France
k
Departement de gynecologie-obstetrique, hopitaux universitaires de Strasbourg, Strasbourg, France
l
Maternite Port-Royal, groupe hospitalier Cochin hotel-Dieu, Paris, France
m
Clinique dobstetrique, pole femme me`re-nouveau-ne, hopital Jeanne-de-Flandre, CHRU de Lille, Lille, France
n
Cytogenetique, hopital universitaire Necker-Enfants-Malades, Paris, France
o
Service danatomie pathologique, pole biologie pathologie, hopital Morvan, CHRU de Brest, Brest, France
p
Service de gynecologie obstetrique, CHU Pitie-Salpetrie`re, Paris, France
q
Pole de gynecologie obstetrique, medecine ftale, medecine et biologie de la reproduction, centre Olympe de Gouges, CHRU de Tours, Tours, France
r
Maternite, hopital universitaire Necker-Enfants-Malades, Paris, France
s
Service de gynecologie-obstetrique, hopital Bicetre, Le Kremlin-Bicetre, France
t
Service de reanimation neonatale, hopital Jeanne-de-Flandre, CHRU de Lille, Lille, France
u
Unite dobstetrique maternite, hopital Trousseau, Assistance Publique Hopitaux de Paris, universite Pierre-et-Marie-Curie-Paris 6, France

A R T I C L E I N F O A B S T R A C T

Article history: Small for gestational age (SGA) is dened by weight (in utero estimated fetal weight or birth weight)
Received 4 October 2014 below the 10th percentile (professional consensus). Severe SGA is SGA below the third percentile
Received in revised form 22 April 2015 (professional consensus). Fetal growth restriction (FGR) or intra-uterine growth restriction (IUGR)
Accepted 25 June 2015
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
Keywords: longitudinally (at least two measurements, 3 weeks apart) (professional consensus). More rarely, they
Small for gestational age
may correspond with inadequate growth, with weight near the 10th percentile without being SGA (LE2).
Fetal growth restriction
Birthweight curves are not appropriate for the identication of SGA at early gestational ages because of
Adjusted fetal weight curves
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
benets 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 decits, school problems and
metabolic syndrome in adulthood. The role of preterm delivery in these complications is linked.

* Corresponding author at: Hopital Paule de Viguier, CHU Toulouse, 330 av de Grande Bretagne, 31059 Toulouse, France. Tel.: +33 567771216; fax: +33 567771219.
E-mail address: christophe.vayssiere@gmail.com (C. Vayssie`re).

http://dx.doi.org/10.1016/j.ejogrb.2015.06.021
0301-2115/ 2015 Elsevier Ireland Ltd. All rights reserved.
 C. Vayssie`re et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 193 (2015) 1018 11

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. Hadlocks
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). Verication of the date of conception is
essential. It is based on the crownrump 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 dEchographie 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 rst-
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 3233 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 3234 weeks of gestation (absent or reversed umbilical end-diastolic ow, 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 insufator, 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 fth
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 100160 mg/day
(Grade A).
2015 Elsevier Ireland Ltd. All rights reserved.

Methods [13]
The sponsor, the French College of Gynaecologists and
Obstetricians, appointed an organization committee (see
Appendix A) to dene 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 scientic 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 Gynecol-
ogists [4] and the Royal College of Obstetricians and Gynaecol-
ogists [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 bibliogra-
phies of identied articles.
For each question, each overview of validated scientic date
was associated with a level of evidence according to the quality of
available data using the working framework dened 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: casecontrol 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 dened by the
HAS as follows.
Classication of recommendations
Grade A: recommendations based on good and consistent
scientic evidence.
12 C. Vayssie`re et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 193 (2015) 1018
Grade B: recommendations based on limited or inconsistent
scientic evidence.
Grade C: recommendations based primarily on consensus and
expert opinion.
Professional consensus: in the absence of any conclusive
scientic 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 establish-
ments)]. Following completion of the review process, changes
were made, if appropriate, considering assessment of the quality of
evidence.
The texts are cited [313], but the individual references
included in each text are not reported here due to space
constraints.
Denitions, 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 pro-
cesses involved. All professionals will also benet from the
adoption of a common language based on specic denitions.
The clearest possible information must be provided to parents to
enable their informed involvement in medical decisions before
and after the birth.
The denition of abnormal growth and the choice of a weight
curve are the main determinants of screening for, and diagnosis
of, FGR.
Denitions
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 dened 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 abnor-
mal 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 uid 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 identication 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 inuence fetal weight
signicantly; 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 dened 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 dened 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 reclassied, 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, ultrasono-
graphers, 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 benets 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 2030 years (LE2).
 Primiparity and grand multiparity double the risk of SGA (LE23).
 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 doseeffect 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 disadvan-
taged 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 difculty 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).
 C. Vayssie`re et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 193 (2015) 1018
 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 613 years of age (LE2).
 As with normal-sized children, the mothers 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
deciencies, symptoms of hyperactivity and attention decit
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 decits, 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 justies 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 dened 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. Hadlocks 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 compara-
ble) (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).
13
 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.
 Verication of the date of conception is essential. This is based on
the crownrump 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
Colle`ge Francais dechographie Ftale data because these are
multicentre French curves (professional consensus).
 Professional practice evaluation of the techniques and distribu-
tion 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, specicity 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 specicity (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 abnormali-
ties, 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 fth percentile (or at least when the abdominal circumfer-
ence is below the 10th percentile) (professional consensus).
 Coordination and homogenization of practices within care
networks are recommended, working with the prenatal diag-
nostic 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 ow (professional consensus).
 The work-up must review the principal items in the history and
clinical ndings (professional consensus).
14 C. Vayssie`re et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 193 (2015) 1018
 An ultrasound will be performed to conrm and specify the
biometric abnormalities and to search for other abnormalities of
the fetus, amniotic uid, placenta and Doppler results.
 Screening for maternalfetal 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 difculty 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 specic
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 uid;
 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 ndings
(professional consensus).
Available surveillance tools
 Umbilical artery Doppler velocimetry and fetal cardiotocography
are the rst-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 insufcient 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 vari-
ability 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 rst-line tool for surveillance of fetuses with SGA
and FGR (professional consensus).
 Despite the absence of randomized trials to demonstrate
potential clinical benets, 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 rst in the arterial
Doppler index, then the venous Doppler index and nally 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 3233 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 23 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 veloci-
metry 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 fth
percentile is considered routinely for management. This
surveillance can be performed on an outpatient basis (profes-
sional consensus).
 In the case of absent diastole or reverse ow on the umbilical
artery Doppler velocimetry, hospitalization must be considered
to administer a course of corticosteroids and organize surveil-
lance, or even delivery. FHR should then be performed daily
(professional consensus).
Indications for immediate delivery
 Before 32 weeks (Fig. 1).
 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 decelera-
tions) 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).
 After 32 weeks (Fig. 2).
 The two possible options are delivery or expectant management
(Grade B).
 In cases of reverse ow 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 ow, 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 uid and Doppler measurements.
The route of delivery will take maternal and obstetric
 C. Vayssie`re et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 193 (2015) 1018 15

Gestational age
EFW
AFI
Umbilical and Cerebral Artery Doppler

Normal UAD

Biometry and UAD

every 2 to 3 weeks
Reduced end-diastolic flow in the UA

Normal CAD Abnormal CAD

UAD and CAD UAD

FHR and/or Computerized FHR with STV FHR and/or Computerized FHR with STV
1 / week 1 / week or more

UAD, umbilical artery doppler; EFW, estimated fetal weight; AFI, amniotic fluid index; CAD,
cerebral artery Doppler; FHR, fetal heart rate; STV, short-term variability.

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

Gestational age
EFW
AFI
UAD and CAD
Absent or reversed end-diastolic flow in the UA

+/- Hospitalization
Corticosteroids

Visual FHR and Computerized FHR with STV every day

Ductus Venosus numerous times a week

Normal FHR Decreased Variability

Normal STV < 5 mn > 40 mn STV < 3 ms ARED on DV
Normal DV and/or
Repeat Decelerations

Continue Cesarean Delivery

surveillance

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.

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

characteristics (parity, previous caesarean, body mass index,
local cervical condition) into account (Grade C).
Role of termination of pregnancy and palliative care in cases of
fetal or intra-uterine vascular growth restriction [14]
 when fetal prognosis appears so compromised that the newborns
chances of survival in good conditions appear very low; and
 when the mothers life is endangered, most often because of pre-
eclampsia.
Gestational age and weight are two major prognostic criteria
(LE1).

Two circumstances can raise the question of termination of  The prognostic assessment is based essentially on ultrasound,
pregnancy in vascular FGR: which must be performed by a senior physician. EFW, growth
16 C. Vayssie`re et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 193 (2015) 1018
rate, fetal Doppler ndings 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 difcult to
predict (professional consensus).
 The couple may also prefer active management with immedi-
ate 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 couples 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 justies 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 3234 weeks of
gestation (absent umbilical ow diastolic end ow or reverse
ow, 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 consen-
sus).
 Caesareans are habitual at early term or in cases of severe
abnormalities of the umbilical artery Doppler velocimetry
(absent diastolic index or reverse ow), 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 ow
on the umbilical artery Doppler) (professional consensus).
 After placement of the prostaglandins or of an intracervical
balloon, surveillance must continue beyond the rst 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 obstetri-
cian 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 (particu-
larly 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 signicantly 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
 C. Vayssie`re et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 193 (2015) 1018
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 insufator, if necessary,
and close monitoring of capillary blood glucose (professional
consensus).
 Transfer to a special unit, especially in a different facility,
depends on the infants 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 compati-
ble with placental vascular insufciency of maternal origin:
 infarction;
 decidual arterial disease;
 syncytial clusters; and
 villous chorangiosis.
 These lesions are variable, non-specic and most suggestive
when they are found together (expert opinion).
 There are other placental diseases that can cause IUGR, including
abnormalities of the conguration 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 rst 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 particular-
ly 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).
17
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 hypo-
glycaemia (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 (profes-
sional 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 previ-
ous 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 1823 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 fth 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 100160 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.
Appendix A
A.1. Steering committee
B. CARBONNE, President (gynaecologist/obstetrician, Hopital
Trousseau, Paris, France), C. VAYSSIERE, Coordinator (gynaecologist/
18 C. Vayssie`re et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 193 (2015) 1018
obstetrician, CHU Toulouse, Toulouse, France), L. SENTILHES, Coordi-
nator (gynaecologist/obstetrician, CHU Angers, Angers, France),
C. ARNAUD, Methodologist (epidemiologist, INSERM U1027, Toulouse,
France), D. COMBOURIEU (Colle`ge Francais dechographie Ftale, Lyon,
France), V. TESSIER (midwife, CNSF, CHU Bicetre, Le Kremlin-Bicetre,
France), B. LANGER (gynaecologist/obstetrician, Societe Francaise de
Medecine Perinatale, CHU Hautepierre, Strasbourg, France), P. TRUF-
FERT (neonatologist, Societe Francaise de Neonatologie, 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.
GRANGE (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 Pitie,
Paris, France), F. PERROTIN (gynaecologist/obstetrician, CHU Tours,
Tours, Paris), L. SALOMON (gynaecologist/obstetrician, CHU Necker,
Paris, France), M.V. SENAT (gynaecologist/obstetrician, CHU Bicetre,
Le Kremlin-Bicetre, Paris) and V. TSATSARIS (gynaecologist/obstetri-
cian, 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 Mater-
nite, 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, Hopital 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/obste-
trician, 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 Lariboisie`re,
Paris, France), V. RIGOURD (paediatrician, Paris, France), C. ROUIL-
LARD (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
[1] Vayssie`re C, Arnaud C, Carbonne B, Sentilhes L. Intrauterine growth retarda-
tion: guidelines for clinical practice: method and organization. J Gynecol
Obstet Biol Reprod 2013;42:8689.
[2] Haute Autorite de Sante AS. Les recommandations pour la pratique clinique.
Base methodologique pour la realisation en France. Saint-Denis La Plaine: HAS;
2011, Available at: http://www.has-sante.fr/portail/jcms/c_431294/les-
recommandations-pour-la-pratique-clinique-base-methodologique-pour-
leur-realisation-en-france (last accessed 24.06.15).
[3] Carbonne B, Sentilhes L, Vayssie`re C. Intrauterine growth retardation: guide-
lines for clinical practice: introduction. J Gynecol Obstet Biol Reprod 2013;42:
8689.
[4] American College of Obstetricians and Gynecologists. Intrauterine growth
restriction. Washington, DC: ACOG; 2000.
[5] Royal College of Obstetricians and Gynecologists. The investigation and man-
agement of the small-for-gestational-age fetus. Guideline No. 31. London:
RCOG; 2002.
[6] Chauhan SP, Gupta LM, Hendrix NW, et al. Intrauterine growth restriction:
comparison of American College of Obstetricians and Gynecologists practice
bulletin with other national guidelines. Am J Obstet Gynecol 2009;200(409):
e16.
[7] Mandruzzato G, Antsaklis A, Botet F, et al. Intrauterine growth restriction
(IUGR). J Perinat Med 2008;36:27781.
[8] Ego A. Denitions: small for gestational age and intrauterine growth retarda-
tion. J Gynecol Obstet Biol Reprod 2013;42:87294.
[9] Gaudineau A. Prevalence, risk factors, maternal and fetal morbidity and
mortality of intrauterine growth restriction and small-for-gestational age. J
Gynecol Obstet Biol Reprod 2013;42:895910.
[10] Gascoin G, Flamant C. Long-term outcome in context of intrauterine growth
restriction and/or small for gestational age newborns. J Gynecol Obstet Biol
Reprod 2013;42:91120.
[11] Grange G. Screening and diagnosis of small for gestational age fetuses. J
Gynecol Obstet Biol Reprod 2013;42:9218.
[12] Salomon LJ, Malan V. Managing and identifying the cause of IUGR. J Gynecol
Obstet Biol Reprod 2013;42:92940.
[13] Senat MV, Tsatsaris V. Prenatal management of isolated IUGR. J Gynecol Obstet
Biol Reprod 2013;42:94165.
[14] Houfin-Debarge V, Azria E. Termination of pregnancy and palliative care in
case of vascular intrauterine growth retardation. J Gynecol Obstet Biol Reprod
2013;42:96674.
[15] Perrotin F, Simon EG, Potin J, Laffon M. Delivery of the IUGR fetus. J Gynecol
Obstet Biol Reprod 2013;42:97584.
[16] Flamant C, Gascoin G. Short-term outcome and small for gestational age
newborn management. J Gynecol Obstet Biol Reprod 2013;42:98595.
[17] Marcorelles P. Placental features in intrauterine growth retardation. J Gynecol
Obstet Biol Reprod 2013;42:9961007.
[18] Nizard J. Prevention of IUGR. J Gynecol Obstet Biol Reprod 2013;42:100817.