Article in press - uncorrected proof

J. Perinat. Med. 36 (2008) 277–281 • Copyright
by Walter de Gruyter • Berlin • New York. DOI 10.1515/JPM.2008.050

Recommendations and guidelines for perinatal practice

Intrauterine restriction (IUGR)*

Giampaolo Mandruzzato1,**, Aris Antsaklis2, assistance can be provided. Careful monitoring of the
Francesc Botet3, Frank A. Chervenak4, IUGR fetus during labor is crucial as the IUGR fetus can
Francisc Figueras5, Amos Grunebaum4, Bienve quickly decompensate once uterine contractions have
Puerto5, Daniel Skupski4,6 and Milan Stanojevic7 started.
1
Department of Obstetrics and Gynecology, Istituto per Keywords: Fetal assessment; IURG; neonatal outcome;
l’Infanzia, Burlo Garofolo, Trieste, Italy SGA.
2
Department Obstetrics and Gynecology, Alexandra
Hospital, University of Athens, Greece
3
Neonatology Service, Hospital Clinic, Institut Clinic, Introduction
Ostetrica, Ginecologia, Neonatologia, Universidad de
Barcelona, Spain Fetal or intrauterine growth restriction (IUGR) is associ-
4
Weill Medical College of Cornell University, New York, ated with perinatal mortality and morbidity. A satisfactory
USA and New York Hospital, Queens, New York, USA definition of IUGR has been suggested by the American
5
Fetal medicine Service, Hospital Clinic, Institut Clinic College of Obstetricians and Gynecologists (ACOG) w1x
as describing ‘‘a fetus that fails to reach his potential
Obstetricia, Ginecologia, Neonatologia, Universidada
growth’’. Small for gestational age (SGA), on the other
de Barcelona, Spain
hand, is a different entity, but is also associated with poor
6
New York Hospital, Queens, New York, USA
perinatal outcomes. SGA is defined as a birth weight
7
Department Obstetrics and Gynecology, Medical
(BW) below a given (usually) the 10th percentile for ges-
School of University of Zagreb, Sveti Duh General
tational age. SGA and IUGR are not synonymous w2, 34,
Hospital, Zagreb, Croatia 45x. The term IUGR should be used only in regard to the
fetus whereas SGA should be used mainly in the new-
Abstract born (but it can be estimated from sonographic meas-
urements of the fetus). IUGR is ideally detected by a
Perinatal mortality and morbidity is markedly increased
diminished growth velocity of the fetus on serial ultra-
in intrauterine growth restricted (IUGR) fetuses. Prenatal
sonographic scans w23x. In this way, the function of
identification of IUGR is the first step in clinical manage-
growth becomes the object of interest instead of the
ment. For that purpose a uniform definition and criteria
result (i.e., birth weight).
are required. The etiology of IUGR is multifactorial and
IUGR is an important clinical problem. The prevalence
whenever possible it should be assessed. When the
is about 8% in the general population. It has been shown
cause is of placental origin, it is possible to identify the
that 52% of stillbirths are associated with IUGR w12x and
affected fetuses. The major complication is chronic fetal
10% of perinatal mortality is a consequence of IUGR
hypoxemia. By monitoring the changes of fetal vital func-
w40x. Up to 72% of unexplained fetal deaths are associ-
tions it is thus possible to improve both management and
ated with SGA below the 10th percentile w14x. The aim of
outcome. The timing of delivery is crucial but the optimal
this document is to review and emphasize important
management scheme has not yet been identified. When
aspects of the identification and management of IUGR.
IUGR is identified at very early gestational ages, serial
IUGR is a condition with an increased risk of a patho-
assessments of the risk of continuing the in utero fetal
logical condition that adversely affects the inherent
life under adverse conditions versus the risks of the pre-
potential growth of the fetus.
maturity should be performed. Delivery of IUGR fetuses
Ideally, the diagnosis of IUGR is a two-step procedure:
should take place in centers where appropriate neonatal
1) restriction of the growth restriction by ultrasonography,
*This paper was produced under the auspices of the WAPM for and 2) identification of a specific cause.
a consensus on issues in perinatal practice, coordinated by
Giampaolo Mandruzzato, MD.
**Corresponding author:
Giampaolo Mandruzzato, MD Recognition
Via del Lazzaretto vecchio 9
34132 Trieste
Italy The recognition of IUGR begins with an accurate gesta-
E-mail: mandruzzatogiampaolo@tin.it tional age (GA). This is best determined by measuring the
 Article in press - uncorrected proof
278 Mandruzzato et al., Intrauterine restriction (IUGR)
crown rump length (CRL) by ultrasound in early pregnan-
cy. Serial ultrasound biometries may then be able to iden-
tify the fetus that does not reach its growth potential.
Commonly used methods for estimating fetal size are
clinical palpation, fundal height (FH) measurement and
ultrasonic fetal biometry. Ultrasound must be considered
the method of choice as it is highly reliable and repro-
ducible w38x. The commonly used ultrasound biometric
parameters in the late 2nd and during the 3rd trimester are
the biparietal diameter (BPD), head circumference (HC),
abdominal circumference (AC) and femur length (FL).
From these measurements the estimated fetal weight
(EFW) can be calculated. The method-error for estimating
fetal weight is 7–10% w20, 43x. Fetuses that do not reach
their growth potential will still have cerebellar growth until
late in the process of IUGR w8x.
When gestational age is questionable, the use of the
transcerebellar diameter (TCD) may be helpful. AC should
be considered as the best single measurement to screen
for poor growth because of its good correlation with fetal
weight w44x. Selecting a threshold of the 10th percentile
for a biometric parameter such as AC or EFW for sus-
pecting or diagnosing IUGR may be a translation of the
postnatal SGA newborn concept into fetal life, which is
undesirable because it may allow fetuses with restricted
growth to be missed if the EFW or AC are above the
selected threshold. Uniform criteria for defining a fetus
as growth restricted on the basis of biometric parameters
are not available, but it is common to use 1.5, 2 or 2.5
SD below the mean for any biometric parameter or com-
bination of parameters w7, 46x. At present, it seems advis-
able to suspect IUGR when the AC measurement deviate
10% or more from the expected from the individual
projected curve of growth.
Ideally, early identification of the fetus that does not
reach its growth potential should employ population spe-
cific growth charts that also take into account other fac-
tors influencing fetal growth. Customized growth charts
also built on homogeneous populations are available and
should be used preferentially in order to decrease the
rate of false positive diagnoses of IUGR w9, 13, 22, 24,
36, 37, 42x. Successive measurements should be carried
not -2 weeks apart w31, 35x. Growth rate tables that take
into consideration the time intervals between measure-
ments can also be used w32x. The evaluation of growth
velocity with serial measurements offers insight into the
characteristics of the growth process and is correlated
with perinatal outcomes w10x.
Etiology
When IUGR is suspected or diagnosed, it is necessary
to distinguish between fetuses that are small but other-
wise healthy (i.e., constitutional small, and therefore not
growth restricted) and those that are a consequence of
an abnormal condition such as a maternal condition
(chronic hypertension, pre-gestational diabetes, cardio-
vascular disease, substance abuse, autoimmune condi-
tions, etc.), a fetal condition (infection, malformation,
chromosomal aberration, etc.), or a placental condition
(chorioangioma, infarction, circumvallate placenta, con-
fined placental mosaicism, obliterative vasculopathy of
the placental bed, etc.). Placental conditions are the most
frequent etiology of IUGR.
Screening
IUGR is a prevalent and significant public health problem
worldwide. In many European countries, four scans are
routinely offered during pregnancy and thus screening for
IUGR is possible at an early gestational age. The diag-
nosis of IUGR is non-invasive with few adverse effects,
treatment may be available, and early detection and
delivery have the potential to improve outcomes w25, 30x.
Prevention
Methods of proven efficacy for preventing IUGR are not
available. Simple means for preventing this problem are
unlikely to be successful because of the multifactorial
nature of IUGR. Chronic fetal hypoxemia (CFH) is
encountered in about 30% of IUGR, suggesting that pre-
vention of the adverse consequences may be possible
after the diagnosis of IUGR w28x. There is some evidence
to suggest that perinatal outcome can be improved by
optimizing the timing of the delivery.
Obstetrical management
Obstetrical management depends on the etiology of
IUGR. For maternal conditions, such as preeclampsia,
management is entirely dependent on the severity of
maternal disease.
When the etiology is of fetal origin, management may
be limited to avoiding prematurity and maternal morbi-
dity. When IUGR is the consequence of a placental etio-
logy (placental insufficiency), management is based on
careful fetal assessment in order to detect the optimal
time for delivery. The most commonly used methods of
monitoring include Doppler flowmetry, cardiotochogra-
phy, amniotic fluid volume evaluation, fetal biophysical
profile and fetal movement counts. Antepartum cardio-
tochography (CTG), alone or as a part of the fetal bio-
physical profile, is almost universally used. In order to
overcome the great intra- and inter-observer variation in
CTG evaluation, computer assisted online evaluation of
short fetal heart rate variability is available and offers a
more precise prediction of fetal acidemia or demise.
 Article in press - uncorrected proof
Doppler velocity waveform in arteries is mainly influ-
enced by the characteristics of the diastolic phase and
reflects the peripheral resistance to blood flow. The pul-
satility index (PI) assessment is commonly used. PI val-
ues increase as the peripheral resistance increases. In
severe IUGR absence of flow in diastole or reverse flow
(ARED) can be observed. Perinatal mortality and morbi-
dity are markedly increased in the presence of ARED flow
w27x. Study of the umbilical artery Doppler waveforms is
fundamental for the identification of restricted blood sup-
ply (placental insufficiency) to the IUGR fetus and evi-
dence suggests that assessment of umbilical artery
Doppler may improve perinatal outcome w33x. Assess-
ment of the Doppler characteristics of the venous sys-
tem, especially the fetal ductus venosus, may also
predict adverse outcomes w5, 11, 29, 48x. At present, the
best way to detect the optimal timing of delivery based
on venous Doppler findings is a matter of debate w18,
39x.
There is no evidence that one monitoring method is
superior to another.
Based on the best available studies, IUGR can be
characterized into several categories on the basis of the
ultrasound findings and gestational age, and the follow-
ing management is suggested.
1. IUGR with normal umbilical artery Doppler wave-
forms and reassuring tests of fetal well-being
– Serial biometry, umbilical Doppler and tests of
fetal well-being.
2. IUGR with umbilical artery PI )2 SD above the mean
for gestational age, presence of diastolic flow and
reassuring tests of fetal well-being
A. Gestational age )34 weeks.
– Umbilical artery Doppler and tests of fetal
well-being twice weekly. Decision for delivery
is based on tests results. Trial of labor for
vaginal delivery is acceptable.
B. Gestational age -34 weeks.
– Umbilical artery Doppler and tests of fetal
well-being twice weekly. Consider corticoste-
roid administration for fetal lung maturation.
Decision for delivery is based on test results.
Trial of labor for vaginal delivery is acceptable.
3. IUGR with umbilical artery PI )2 SD above the mean
for gestational age, presence of diastolic flow and
non-reassuring tests of fetal well-being
A. Gestational age )34 weeks.
– Daily umbilical artery Doppler and daily tests
of fetal well-being. Consider delivery. Trial of
labor for vaginal delivery is acceptable.
B. Gestational age -34 weeks.
– Corticosteroid administration for fetal lung
maturation. Daily umbilical artery Doppler and
daily tests of fetal well-being. Consider deliv-
Mandruzzato et al., Intrauterine restriction (IUGR) 279
ery. Trial of labor for vaginal delivery is
acceptable.
4. IUGR with umbilical artery absent diastolic flow. Tests
of fetal well-being are usually non-reassuring.
A. Gestational age )34 weeks.
– Consider delivery
B. Gestational age -34 weeks.
– Corticosteroid administration for fetal lung
maturation. Consider delivery.
5. IUGR with reversed diastolic flow in the umbilical
artery. Tests of fetal well-being are nearly always non-
reassuring.
A. Gestational age )34 weeks.
– Extensive counselling on mortality and mor-
bidity. Active or expectant management
according to the choice of the family.
B. Gestational age -34 weeks.
– Extensive counselling on mortality and mor-
bidity. Active or expectant management
according to the choice of the family in con-
cert with the obstetric and neonatal teams.
Corticosteroid administration for fetal lung
maturation.
Before 33–34 weeks, delivery is a compromise between
the risks of fetal demise with continued in utero life under
adverse conditions and the risk of severe prematurity.
Antenatal corticosteroids administration has a positive
effect for both the short- and long-term complications.
Clinicians should remember that steroid (betamethazone)
administration reduces FHR variability and the number
of accelerations. The FHR pattern should be carefully
assessed after steroid administration to avoid unwar-
ranted iatrogenic delivery w41x. Counselling must be
informative and non-directive, respecting the principle of
autonomy of the mother.
Delivery of the IUGR fetus is best performed at a cen-
ter where intensive neonatal assistance is available. The
delivery mode depends on the fetal condition appreci-
ated from fetal evaluations and the tolerance of the fetus
to labor. It is not always necessary to perform cesarean
delivery for fetuses with IUGR. Also in presence of umbil-
ical artery PI over 2 SD safe vaginal delivery, under close
monitoring, can be achieved in 24–40% of the cases w21,
28x. The more pronounced the hypoxemia and acidemia,
the more likely the fetus will not tolerate labor and it is
less likely that vaginal delivery will be a safe option. IUGR
fetuses from a placental or maternal condition are less
likely to tolerate labor than those from fetal conditions.
Neonatal management
Infants born after IUGR may have significant morbidity,
including metabolic (hypoglycemia, dislipidemia), hema-
 Article in press - uncorrected proof
280 Mandruzzato et al., Intrauterine restriction (IUGR)
tologic (elevated nucleated red blood cells count) and
cardiovascular disorders (hypotension). Subcutaneous
fat and glycogen stores are almost universally depleted.
Precocious feeding with 110–165 kcal/kg/day is recom-
mended by breast feeding if at all possible. The devel-
opment of necrotizing enterocolitis, which can occur as
a consequence of blood flow redistribution and reduced
supply to the gut, should be looked for. Controversy
exists regarding the effect of IUGR on the incidence of
intraventricular hemorrhage w3, 15, 19x. Cognitive func-
tion seems to be affected w16, 17x. Recent neuroimaging
studies have shown altered development of cerebral
structures w6, 26, 47x. Early cranial ultrasound and MR
imaging are recommended.
Recommendations
1. The terms IUGR and SGA are not synonymous.
IUGR is used for the fetus and SGA is used primarily
for the newborn. (Level A)
2. IUGR should be defined on the basis of serial meas-
urements showing restricted growth. (Level B)
3. Abdominal circumference measurements are easy to
perform and can be used for growth assessment.
(Level B)
4. Customized, population-specific growth charts
should be used when possible. (Level B)
5. The timely recognition of IUGR improves both man-
agement and outcomes. Screening for IUGR should
be considered. (Level A)
6. When IUGR is suspected, the etiology should be
explored. (Level B)
7. When the etiology is thought to be placental, Dopp-
ler study of the umbilical artery allows the identifi-
cation or exclusion of significant chronic fetal
hypoxemia. Close monitoring of Doppler blood flow
changes should guide clinical management. (Level
A)
8. There is no evidence that one type of monitoring is
superior to another. Serial fetal assessment is opti-
mal to identify the best time for delivery. (Level B)
9. Careful monitoring of the IUGR fetus in labor is cru-
cial as a rapid deterioration is possible with uterine
contractions. (Level B)
10. Detailed counselling with the family that includes the
obstetrician and the neonatologist is recommended.
(Level C)
11. Delivery of IUGR should take place where an appro-
priate neonatal care is available. In utero transport
should be preferred. (Level B)
12. After delivery of a neonate with IUGR, early neuro-
imaging is recommended. (Level B)
13. There is no effective management for the prevention
or in utero treatment of IUGR. In case of CFH the
only effective therapy is delivery. (Level B)
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Previously published online May 24, 2008.