European Journal of Obstetrics & Gynecology and Reproductive Biology 171 (2013) 257261

Contents lists available at ScienceDirect

European Journal of Obstetrics & Gynecology and

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

Induction of labor for term small-for-gestational-age fetuses:

what are the consequences?
Keren Or a, Liat Lerner-Geva b,c, Valentina Boyko b, Eran Zilberberg a, Eyal Schiff a,c,
Michal J. Simchen a,c,*
a
Department of Obstetrics and Gynecology, Sheba Medical Center, Tel Hashomer, Israel
b
Women and Childrens Health Research Unit, The Gertner Institute for Epidemiology and Health Policy Research Ltd., Tel Hashomer, Israel
c
Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel

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

Article history: Objective: To evaluate whether early term labor induction for suspected intrauterine growth restriction
Received 23 April 2013 (weeks 3739) improves neonatal outcome for small-for-gestational-age (SGA) neonates.
Received in revised form 21 August 2013 Study design: Delivery room data for 20042008 from a single tertiary medical center were linked to
Accepted 15 September 2013
neonatal discharge data from the same institution. Data were limited to all singleton, liveborn SGA
neonates born at 3742 weeks of gestation and their mothers. Births with known congenital anomalies
Keywords: were excluded. Women undergoing induction of labor for suspected growth restriction between 37 and
SGA
39 weeks gestation (early induction SGA) were compared with women who gave birth to term SGA
Small for gestational age
Induction of labor
neonates without early induction. SGA (<10th percentile for gestational age and gender) was used as a
Term SGA surrogate for intrauterine growth restriction. Associations between early term labor induction and
neonatal morbidities were estimated using logistic regression.
Results: A total of 2378 SGA neonates meeting study criteria were identied. Of these, 445 underwent
early term induction and 1933 were in the non-early induction SGA group. Intrauterine demise among
term (3742 weeks) SGAs occurred in one case at 37 weeks. Early term induction for SGA was associated
with an increased risk of cesarean delivery. Several neonatal complications, including hyperbilir-
ubinemia, hypoglycemia and respiratory complications were more prevalent in the early induction SGA
group. The increased odds for neonatal complications persisted after controlling for possible
confounders.
Conclusions: Early term induction for SGA fetuses results in an increased risk of cesarean deliveries as
well as neonatal metabolic and respiratory complications, with no apparent neonatal benet.
2013 Elsevier Ireland Ltd. All rights reserved.

1. Introduction
Information on short- and long-term consequences of small-
for-gestational-age (SGA, birthweight <10th percentile for gesta-
tional age) neonates at term is inconsistent. Most of the data
suggest an increased rate of immediate complications, short-term
morbidity and mortality [13], as well as long-term neurological
and cognitive developmental delays in childhood [4,5]. Not all
studies, however, conrm these ndings [610].
The majority (approximately 80%) of all SGA neonates are born
at term [11]. A clinical dilemma arises regarding induction of labor
in cases in which the fetus appears small-for-dates toward term, as
* Corresponding author at: Department of Obstetrics and Gynecology, Sheba
Medical Center, Tel Hashomer 52621, Israel. Tel.: +972 3 5302169;
fax: +972 3 5302922.
E-mail addresses: michal.simchen@sheba.health.gov.il,
mnir_simchen@hotmail.com (M.J. Simchen).
most of the neonates with birth weight below the 10th percentile
are part of the normal spectrum of fetal growth, rather than being
abnormally small because of a compromised intrauterine envi-
ronment [12]. On the one hand, accelerating delivery may improve
perinatal outcome and prevent the peril of fetal demise. If, on the
other hand, these fetuses are small as a variant of the normal range,
early induction of delivery may not improve their outcome and
might lead to a rise in obstetric complications. A few retrospective
studies [1319], as well as a recent multicenter prospective study
[20], investigated neonatal and maternal outcomes following
induction of labor of fetuses with intrauterine growth restriction
(IUGR) at term. Conicting ndings are reported, however,
regarding neonatal benets and the rate of obstetrical interven-
tions.
We aimed to investigate the impact of early induction of labor
on neonatal outcome and on the rate of maternal obstetrical
interventions in a large cohort of SGA term infants at a single
center.

0301-2115/$ see front matter 2013 Elsevier Ireland Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ejogrb.2013.09.016
258 K. Or et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 171 (2013) 257261
2. Methods
The study cohort included all term singleton deliveries and
respective neonatal outcomes occurring between 1st August 2004
and 30th September 2008 at Sheba Medical Center, Israel. During
this time frame, one of the management options for pre-identied
SGA fetuses was induction of labor at 3738 weeks in order to
minimize risks of fetal compromise and possible fetal demise while
awaiting spontaneous labor.
Data on all births were prospectively entered into a computer-
ized database by the obstetrician or midwife attending to the
laboring woman and responsible for her medical care. The
information entered into this database included maternal demo-
graphics, obstetrical history, labor and delivery events and
immediate neonatal outcome. In most cases, a rst-trimester
ultrasound scan was used for gestational age dating. When
ultrasound dating was discordant with last menstrual period by
7 days or more, ultrasound dating only was used to calculate
gestational age. A last-menstrual-period only dating was used for
the minority of women for whom rst-trimester sonography was
not available. The post-delivery medical course was also entered
into the same database. This database was cross-linked to all in-
hospital events and nal diagnoses for liveborn neonates born
during the study period, as recorded by the treating neonatologist
upon discharge.
For the current analyses we investigated maternal and neonatal
outcome of term (3742 weeks gestation) growth-restricted
singleton deliveries. Small-for gestational age (SGA) was used as
a surrogate for growth restriction, and was dened as birth weight
lower than the 10th percentile adjusted for gestational age and
gender according to locally derived references [21].
The exposed group, termed early induction SGA group,
included women giving birth after induction of labor for suspected
IUGR of a singleton SGA neonate between 37 and 39 weeks
gestation. These were fetuses that were recognized antenatally as
being growth restricted. The unexposed group, or no early
induction SGA group consisted of women giving birth at or after
40 weeks gestation, and included also those who gave birth
spontaneously to term SGA neonates at 3739 weeks. The
inclusion of spontaneous deliveries of SGA neonates at 3739
weeks was targeted to minimize differences in morbidity that are
the result of relative immaturity and different gestational ages.
Our aim was to address the benet of active medical
intervention for suspected IUGR among the term SGA cohort
(i.e. induction of labor). The early induction SGA and the no early
induction SGA groups were compared regarding maternal
characteristics, pregnancy and neonatal complications as well
as obstetrical interventions in order to evaluate possible benets
and drawbacks of an early term induction of labor for suspected
IUGR.
Table 1
Maternal obstetric complications and outcomes.
Hypertensive complications
Diabetes mellitus
Placental abruption
Post partum hemorrhage, blood transfusion
Mode of delivery
Spontaneous delivery
Operative delivery
Cesarean section
Post partum hemorrhage, blood transfusion
Maternal infection, post partum fever
SGA small for gestational age.
Exclusion criteria included multifetal pregnancies and neonates
born with major congenital abnormalities. Maternal obstetric data
included maternal age, past medical history, gestational age at
delivery, mode of delivery and major peripartum complications. All
cases of antenatal fetal demise of term SGA fetuses were included
in the analysis.
Neonatal outcomes investigated included: gender of newborn,
1- and 5-min Apgar scores, and adverse neonatal outcomes.
Adverse neonatal outcomes included: neurological complications
(intraventricular hemorrhage, convulsions, asphyxia, acidosis),
gastrointestinal complications (necrotizing enterocolitis, intestinal
perforation), respiratory complications (respiratory distress syn-
drome (RDS), mechanical ventilation), infections, thrombocytope-
nia, blood transfusion, hyperbilirubinemia and phototherapy,
meconium aspiration syndrome, birth trauma (brachial plexus
injury, Erbs palsy, other bone and nerve injury), hypoglycemia,
need for resuscitation and neonatal death. We dened a combined
adverse neonatal outcome variable which included the existence
of at least one of the above mentioned neonatal complications.
Statistical analysis was performed using the SAS statistical
software (Version 9.2, SAS institute, Cary, NC, USA). Continuous
variables were presented as mean  SD and compared using the t-
test. Chi-square test or Fishers exact test were used for comparison of
categorical variables. A two-sided p-value of less than 0.05 was
considered statistically signicant.
Multivariable analyses to determine the independent predic-
tors of neonatal complications were performed by logistic
regression models. Results of the logistic model are presented as
adjusted odds ratios (OR) with 95% condence intervals (CI). In
order to control for possible confounders, adjustment was made
for hypertension, diabetes mellitus, cesarean delivery, SGA
severity, and a combination of induction of labor and gestational
week, or performing induction and gestational week as separate
variables, depending on the model.
The study protocol was approved by the Institutional Review
Board (IRB) at Sheba Medical Center, Tel Hashomer.
3. Results
During the study period 37,342 women gave birth to singleton
neonates at 37 weeks of gestation at Sheba Medical Center. Of
these, 2378 (6.36%) neonates were born small for gestational age.
The early-induction-SGA group consisted of 445 neonates born at
3739 weeks gestation after induction of labor for assumed IUGR,
and the no-early-induction SGA group consisted of 1933 neonates
born at 40 weeks gestation and those born after spontaneous
onset of labor at 3739 weeks.
Maternal age was similar between the groups (30.1  5.1 and
30.3  5.0, respectively). Maternal obstetric complications and out-
comes are outlined in Table 1. Most obstetric complications (placental
Early induction SGA No early induction p-Value
N = 445 N = 1933
n (%) n (%)
20 (4.5) 40 (2.1) 0.006
18 (4.1) 57 (2.9) 0.23
2 (0.45) 5 (0.3) 0.62
2 (0.45) 7 (0.36) 0.68
290 (65.2) 1364 (70.5) <0.0001
27 (6) 200 (10.4)
128 (28.8) 369 (19.1)
2 (0.45) 7 (0.36) 0.68
2 (0.45) 3 (0.2) 0.23
 K. Or et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 171 (2013) 257261 259

Table 2
Pregnancy and immediate neonatal outcomes of the early-induction SGA group and no-early-induction SGA group.

Early induction SGA No early induction SGA p-Value

N = 445 N = 1933
n (%) n (%)

GA at delivery, weeks (mean  SD) 37.9  0.8 39.4  1.1 <0.0001

Birth weight (grams  SD) 2326  211 2624  203 <0.0001
Birth weight <1st percentile 37 (8.3) 74 (3.8) <0.0001
Newborn gender male 222 (49.9) 984 (50.9) 0.69
Apgar 1 min <7 10 (2.2) 42 (2.2) 0.99
Apgar 5 min <7 2 (0.4) 7 (0.4) 0.68

SGA small for gestational age; GA gestational age; SD standard deviation.

abruption, diabetes mellitus, postpartum hemorrhage, etc.) were
similar between the two groups. Women in the early induction SGA
group had signicantly more hypertensive complications compared
with women in the unexposed group (Table 1).
Additionally, mothers undergoing early induction of labor for
SGA had a higher rate of cesarean deliveries compared with the
unexposed group women, and only 65.5% of them reached non-
instrumental vaginal delivery (p < 0.0001).
Short-term outcomes such as Apgar scores at 1 and 5 min, as
well as gender, were similar between the exposed and non-
exposed groups (Table 2). Not surprisingly, the early-induction-
SGA neonates were born at an earlier gestational age and had lower
mean birth weights. The proportion of neonates with birth weight
under the 1st percentile for gestational age and gender was higher
among the early induction group compared with non-early-
induction SGAs.
The early induction SGA group had a signicantly higher rate
of neonatal complications compared with no early induction
SGAs. There was a higher rate of hyperbilirubinemia necessitating
phototherapy (OR = 1.75, 95% CI 1.212.53) as well as of
hypoglycemia (OR = 2.38, 95% CI 1.563.62). Two cases of
respiratory complications occurred, both in the early induction
SGA group. Other complications, including necrotizing enterocoli-
tis, sepsis, adverse neurological outcomes and need for resuscita-
tion, were rare and similar in both groups (Table 3). There were no
cases of neonatal death in either group. The risk of any adverse
neonatal outcome (combined adverse neonatal outcome) was
almost 2 times higher for the early induction compared with the
no early induction group (OR = 1.95, 95% CI 1.462.61,
p < 0.0001).
Furthermore, we analyzed the data using multivariable models
in order to control for possible confounders (Table 4). Early
induction of SGA neonates in combination with gestational week
(Model 1) was found to be associated with an increased risk of
neonatal complications (adjusted OR 2.14, 95% CI 1.54; 2.97,
p < 0.0001) after controlling for maternal hypertension, diabetes
and mode of delivery. An increasing severity of growth restriction
(i.e. birth weight less than 1st percentile and between 1st and 5th
percentile) was also signicantly associated with an elevated risk
of neonatal complications.
In order to take into account the higher rate of induction in
earlier gestational age, we analyzed performance of induction and
gestational week as separate variables (Model 2). Both earlier
gestational age and the severity of growth restriction were
signicantly associated with neonatal complications. Performance
of induction of labor was associated with an increased risk for
neonatal complications, although not signicantly (OR = 1.2; 95%
CI 0.851.69). Therefore, the importance of gestational age in
determining neonatal outcome is evident even in the term
neonate.
The most signicant possible hazard of abstaining from
induction of labor for suspected IUGR at term is intrauterine fetal
demise. During the study period there were 33 cases of fetal
demise between 37 and 42 weeks gestation out of 37,342 singleton
deliveries 0.88 cases per 1000 live births at term of which only
one case was an SGA fetus at 37 weeks gestation. Therefore, the risk
of intrauterine fetal demise at term for non-early induction SGAs
was calculated to be 0.52 cases per 1000 live births, which was no
higher than that of the general term population (OR 0.57, 95% CI
0.08, 3.85, p = 0.99).
4. Comments
In the current study we tried to address the timing of delivery
for suspected IUGR at term. On one hand, awaiting spontaneous
labor carries risks of eventual fetal decompensation due to a
possibly compromised intrauterine environment. On the other
hand, active induction of labor might result in an increased rate of

Table 3
Neonatal complications of early induction and no early induction neonates.

Complications Early induction SGA No early induction SGA p-Value

N = 445 N = 1933
n (%) n (%)

Necrotizing Enterocolitis 1 (0.2) 3 (0.2) 0.56

Respiratory complications 2 (0.45) 0 (0) 0.03
Infections 0 (0) 1 (0.05) 0.99
Neurological complications 0 (0) 3 (0.2) 0.99
Thrombocytopenia 1 (0.2) 8 (0.4) 0.99
Blood transfusion 1 (0.2) 2 (0.1) 0.46
Hyperbilirubinemia, phototherapy 47 (10.6) 122 (6.3) 0.003
Meconium aspiration syndrome 0 (0) 2 (0.1) 0.99
Birth trauma 0 (0) 2 (0.1) 0.99
Hypoglycemia 39 (8.8) 75 (3.9) <0.0001
Neonatal resuscitation 0 (0) 4 (0.2) 0.99
Neonatal death 0 (0) 0 (0) 0.99
Combined adverse neonatal outcome (at least one adverse neonatal outcome) 83 (18.6) 203 (10.5) <0.0001

There was one case of intrauterine fetal demise of an SGA fetus (37 weeks).
260 K. Or et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 171 (2013) 257261

Table 4
Multivariable logistic regression model for the prediction of adverse neonatal outcomes.

Variable N Neonatal complication Model 1 Model 2

n (%)
Adjusted OR (95% CI) p-Value Adjusted OR (95%CI) p-Value

Hypertension
No 2318 280 (12.1) 1.0 1.00
Yes 60 6 (10) 0.69 (0.291.63) 0.4 0.66 (0.271.58) 0.35

Diabetes mellitus
No 2303 276 (12.0) 1.0 1.00
Yes 75 10 (13.3) 1.06 (0.532.1) 0.87 1.02 (0.512.04) 0.95

Cesarean section
No 1881 215 (11.4) 1.0 1.00
Yes 497 71 (14.3) 1.15 (0.861.55) 0.34 1.07 (0.801.45) 0.64

IUGR
<1 percentile 111 23 (20.7) 2.07 (1.263.42) 0.004 2.20 (1.333.65) 0.002
15 percentile 857 118 (13.8) 1.31 (1.01.7) 0.04 1.35 (1.031.76) 0.03
510 percentile 1410 145 (10.3) 1.0 1.00

Induction and GA
3739 weeks, Induction 445 83 (18.6) 2.14 (1.542.97) <0.0001
3739 weeks, no induction 929 112 (12.1) 1.40 (1.042.88) 0.02
4042 weeks 1004 91 (9.1) 1.0

Gestational age
37 274 66 (24.1) 3.30 (1.915.68) <0.0001
38 466 60 (12.9) 1.59 (0.952.67) 0.07
39 634 69 (10.9) 1.37 (0.842.23) 0.20
40 659 61 (9.3) 1.21 (0.741.96) 0.45
41 312 25 (8.0) 1.00
42 33 5 (15.2) 1.91 (0.675.41) 0.22

Induction
No 1933 203 (10.5) 1.00
Yes 445 83 (18.6) 1.20 (0.851.69) 0.30

IUGR intrauterine growth restriction; GA gestational age.

obstetrical interventions and neonatal complications of early term
delivery.
The literature addressing the management of term SGA fetuses
is limited. In our study, in order to evaluate whether early term
induction of labor results in fetal, neonatal or maternal benets, we
evaluated nearly 2400 SGA pregnancies 445 which underwent
induction of labor due to suspected growth restriction at 3739
weeks of gestation and 1933 SGA fetuses whose delivery was not
induced at early term. Our results show that induction of labor at
early term for singleton SGA fetuses with suspected growth
restriction results in a higher rate of adverse neonatal outcomes.
This increased risk was dominated by hypoglycemia (close to 50%
of adverse outcomes) that is invariably monitored in SGA fetuses.
Nevertheless, even when this outcome variable was excluded the
increased risk for early induced SGAs was still signicant although
to a lesser extent (OR = 1.55, 95% CI 1.082.22). Other retrospective
studies previously found either worse neonatal outcome or no
benet for the induced SGA term newborns [1315,17,19]. On the
other hand, Lindqvist and Molin [18] found a fourfold increased
risk of adverse neonatal outcome among SGA fetuses unrecognized
before delivery, compared with SGA fetuses that were identied
prior to delivery. That study nevertheless addressed both preterm
and term neonates and found most of the cases with severe
neonatal outcome to be among preterm SGA pregnancies.
In the recently published DIGITAT study [20], 321 IUGR
pregnancies were allocated to labor induction at term and 329
to expectant monitoring. No signicant differences in a composite
adverse neonatal outcome were found between the groups. The
recently published follow-up paper on long-term outcome of
infants participating in the DIGITAT study [22] found no difference
in developmental or behavioral outcomes between the induced
and the expectant management groups at 2 years of age.
Contrary to the DIGITAT study, the present study found a
signicantly higher rate of severe growth restriction (birth weight
less than the 1st percentile) among the early-induction-SGA group.
This difference may be a consequence of the retrospective study
design, in that the more severely growth-restricted fetuses were
recognized earlier. Nevertheless, after adjustment for maternal
hypertension, diabetes, severity of growth restriction and mode of
delivery, our results demonstrated a signicant increase in the
combined adverse neonatal outcome for the early induction SGA
group, emphasizing the negative impact of gestational age on fetal
outcome. Compared with SGA infants born 40 weeks gestation,
SGA infants born spontaneously at 3739 weeks had an odds ratio
of 1.4 for adverse neonatal outcomes, whereas those born at 3739
weeks after labor induction for IUGR had an even higher risk (OR
2.14). Therefore, in the multivariate model early induction of labor
for suspected growth restriction did not confer benets on these
neonates and may have contributed to their adverse outcomes due
to additional immaturity.
Another recently published trial (the HYPITAT study) found
improved maternal outcome with induction of labor at term for
women with mild hypertensive disease but no difference in
neonatal outcome and rates of cesarean section [24]. Nevertheless,
neonates in the HYPITAT study did not have IUGR. Our results in
the present study imply that the added morbidities for the early
induction group stem from their earlier gestational age. Moreover,
we demonstrated that cesarean sections were performed almost
twice as often on mothers whose deliveries were initiated early for
suspected growth restriction compared with non-induced SGAs
(28.8% versus 19.1%). Maslovitz et al. [25] also described a high rate
of non-elective cesarean deliveries in women induced for IUGR,
compared with women induced for other indications. Similar
ndings were also described by others [1319].
 K. Or et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 171 (2013) 257261
Of our term SGA cohort, only one case of in utero demise of an
SGA fetus was identied between 37 and 42 weeks gestation (0.52
cases per 1000 live births), similar to the overall rate of fetal demise
at term. A previous study [23] found that most fetal deaths
resulting from placental insufciency occurred earlier than 37
weeks gestation, possibly indicating that term fetal demise may
result from reasons unrelated to placental function and fetal
growth (i.e. cord accidents, etc.).
A weakness of our study is that data were collected
retrospectively from medical records, and we were therefore
unable to assess the decision-making process during pregnancy.
Possibly, women who undergo surveillance during pregnancy (and
whose fetuses are recognized as IUGR) may be a higher risk group
at baseline for reasons not accounted for by our multivariable
analysis. Nevertheless, it should be noted that over 90% of pregnant
women in central Israel receive prenatal care, and a sonogram in
the late third trimester is part of this assessment. Furthermore, this
retrospective design enabled us to evaluate outcomes in a
relatively large cohort of SGA term pregnancies. We included only
cases with induction of delivery due to suspected growth
restriction, and analyzed pregnancy outcomes of almost 2400
SGA neonates at term. This allowed us to include neonatal
complications that are relatively uncommon in the term popula-
tion. Moreover, the data were obtained during a 4 year period from
a single medical center, when neonatal management did not
change signicantly.
In summary, in this large retrospective cohort analysis we
demonstrate a lack of apparent neonatal benet for early term
induction of labor for SGA neonates, while obstetrical intervention
rates increase. Inducing early term labor at 3739 weeks has
drawbacks and an apparent lack of neonatal benet. Further large
prospective studies are needed in order to assess the optimal
management of the SGA fetus toward term.
Conict of interest
The authors report no conict of interest.
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