Research

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OBSTETRICS

Nonspontaneous late preterm birth: etiology and outcomes

Cynthia Gyamfi-Bannerman, MD; Karin M. Fuchs, MD; Omar M. Young, MD; Matthew K. Hoffman, MD
OBJECTIVE: We sought to determine the proportion of evidence-based

(EB), vs non-EB (NEB) iatrogenic late preterm birth, and to compare corresponding rates of neonatal intensive care unit (NICU) admission.
STUDY DESIGN: We performed a retrospective cohort study. Cases
were categorized as EB or NEB. NICU admission was compared between groups in both univariate and multivariate analysis.
RESULTS: Of 2693 late preterm deliveries, 32.3% (872/2693) were

iatrogenic; 56.7% were delivered for NEB indications. Women with NEB
deliveries were older (30.0 vs 28.6 years, P .001), and more likely to
be pregnant with twins (18.8% vs 7.9%, P .001), have private insur-

ance (80.3% vs 59.0%, P .001), or have a second complicating factor (27.5% vs 10.1%, P .001). A total of 56% of EB deliveries resulted in NICU admissions. After controlling for confounders, early
gestational age (34 vs 36 weeks: odds ratio, 19.34; 95% confidence
interval, 4.28 87.5) and mode of delivery (cesarean: odds ratio, 1.88;
95% confidence interval, 1.153.05) were most strongly associated
with NICU admission.
CONCLUSION: Over half of nonspontaneous late preterm births were

NEB. EB guidelines are needed.

Key words: iatrogenic prematurity, late preterm birth

Cite this article as: Gyamfi-Bannerman C, Fuchs KM, Young OM, et al. Nonspontaneous late preterm birth: etiology and outcomes. Am J Obstet Gynecol
2011;205:456.e1-6.

he morbidity associated with late

preterm birth, defined as birth from
34 0/7-36 6/7 weeks, has recently become
the topic of much debate and literature.1-4 We now understand that late
preterm birth is associated with significantly higher rates of respiratory morbidity, but also results in other morbidi-

From the Division of Maternal-Fetal Medicine,

Department of Obstetrics and Gynecology,
College of Physicians and Surgeons, Columbia
University, New York, NY (Drs GyamfiBannerman and Fuchs); the Department of
Obstetrics and Gynecology, Yale Medical
Center, New Haven, CT (Dr Young); and the
Department of Obstetrics and Gynecology,
Christiana Care Health System, Newark, DE
(Dr Hoffman).
Received March 8, 2011; revised May 24,
2011; accepted August 8, 2011.
The authors report no conflict of interest.
Presented at the 30th annual meeting of the
Society for Maternal-Fetal Medicine, Chicago,
IL, Feb. 1-6, 2010.
Reprints not available from the authors.
0002-9378/free
2011 Mosby, Inc. All rights reserved.
doi: 10.1016/j.ajog.2011.08.007

For Editors Commentary,

see Table of Contents
See related editorial, page 395

456.e1

ties such as intraventricular hemorrhage,

necrotizing enterocolitis, neonatal intensive care unit (NICU) admission, and
sepsis, when compared to infants born at
term. McIntire and Leveno1 compared
the different types of morbidities associated with late preterm birth to birth at 39
weeks, the gestational age with the lowest
morbidity in their cohort of 21,771 deliveries over an 18-year period. They
found that ventilator use, transient tachypnea of the newborn, sepsis, phototherapy
for hyperbilirubinemia, and intraventricular hemorrhage were all significantly higher
in late preterm infants compared to term.
Similarly, Yoder et al2 reviewed the epidemiology of respiratory disease in late preterm infants. They found that respiratory
morbidity from all causes was higher at 34
weeks (22%), 35 weeks (8.5%), and 36
weeks (3.9%) when compared to 39 and
40 weeks (0.7% and 0.8%, respectively,
P .001). These findings were corroborated recently by the Safe Labor Consortium.3 Currently, the standard of care is
not to administer antenatal corticosteroids
to women at risk for late preterm delivery
due to a lack of data showing benefit at
these later gestational ages.
Mortality is known to be higher as
well. Tomashek et al4 and McIntire and
Leveno1 both showed that infant mortal-

American Journal of Obstetrics & Gynecology NOVEMBER 2011

ity was up to 3 times higher after late preterm birth compared to birth at term.
Reddy et al5 found that neonatal mortality and infant mortality were 9.5- and
5.4-fold higher following birth at 34
weeks compared to 39 weeks. The increased morbidity and mortality associated with late preterm birth when compared to term is concerning and raises
the question as to whether the indications for these births are justified.
Additionally, long-term outcomes have
been found to be poorer in late preterm
infants compared to term. Tagle et al6
found that IQ scores were lower at 6 years
of age in children of women with a late preterm birth compared with similar term
children. Another study of preschool and
kindergarten children born late preterm
compared with term children showed that
the late preterm children were more likely
to have developmental delay and suspension and retention in kindergarten.7 Finally, Moster et al8 found that adults born
late preterm in Norway were 2.7 times
more likely to have cerebral palsy and 1.6
times more likely to have mental retardation. These data further question the need
to deliver these infants in the late preterm
period.
In an effort to understand the etiology
of late preterm births at our respective
institutions, we sought to define a cohort
of these deliveries to review indications

Obstetrics

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TABLE 1

Categorization of indications for delivery

Indications for delivery
Evidence based
Severe preeclampsia/eclampsia

Nonevidence based
Chronic hypertension/gestational hypertension/
mild preeclampsia

..............................................................................................................................................................................................................................................

IUGR with abnormal testing or poor

interval growth

IUGR with normal testing and adequate interval

growth

..............................................................................................................................................................................................................................................

Acute abruption

Prior myomectomy/classic cesarean

Nonreassuring fetal heart rate tracing

Oligohydramnios

Cholestasis, bile acids 40 micromol/L

Cholestasis, bile acids 40 micromol/L

Uterine rupture

Elective

..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................

IUGR, intrauterine growth restriction.

Gyamfi-Bannerman. Iatrogenic late preterm birth. Am J Obstet Gynecol 2011.

and neonatal outcomes. Our specific objectives were 3-fold: first, to evaluate the
proportion of late preterm deliveries that
were nonspontaneous (iatrogenic); second, to evaluate the proportion of nonspontaneous deliveries that were based
on evidence as opposed to common local
practice; and third, to identify the indications for late preterm birth that require further research.

M ATERIALS AND M ETHODS

Using 2 contemporaneously maintained obstetrical databases, all women

from Columbia University Medical

Center and Christiana Care Health
System who delivered between 34
0/7-36 6/7 weeks from January 2003
through July 2007 were identified.
Both datasets are entered by individuals who solely perform data abstraction
from medical charts. Prior to data collection the institutional review boards
from both institutions were consulted
and this study was approved by both
via expedited review. Data regarding
indication for delivery were abstracted
from direct chart review.

FIGURE

Diagram of inclusion and exclusion

Gyamfi-Bannerman. Iatrogenic late preterm birth. Am J Obstet Gynecol 2011.

Research

Theprimaryoutcomeofthisstudywasthe
rate of nonspontaneous, late preterm delivery with an indication that was supported by
current evidence as endorsed by the American College of Obstetricians and Gynecologists (ACOG) or published expert opinion
(level III evidence). Spontaneous causes of
preterm delivery were considered to have occurred for women with preterm birth preceded by either preterm premature rupture
of membranes (PPROM) or preterm labor
with intact membranes. Women with
PPROM were considered to have spontaneous preterm labor whether or not labor
induction was performed. Women with
triplet or higher-order multiple gestations
were excluded from all analysis as the optimal period of delivery for these women
remains controversial. Also excluded were
women for whom the indication for delivery was indeterminate. Cases were designated as indeterminate under the following circumstances: (1) the indication was not
identified in the medical record; (2) the indication was an appropriate indication but
the clinical documentation failed to support the given reason (eg, severe preeclampsia with no record of blood pressure
or other support of the diagnosis); or (3)
the 2 reviewers were unable to reach consensus as to the appropriateness of the indication. We did not exclude fetuses with
documented fetal lung maturity because
this has not been shown to improve neonatal outcomes.9
Indications for nonspontaneous deliveries were assessed through review of the
medical records, and 2 authors (M.K.H.
and C.G-B.) independently reviewed
each indication for consensus. Outpatient records were not reviewed. Those
indications supported by ACOG guidelines and/or expert opinion (level C evidence and consensus from obstetric
texts) were defined as evidence based
(EB), while indications not supported by
either of these were labeled non-EB
(NEB). Where multiple indications were
listed, if at least one of the indications
was EB, the patient would be classified as
such. For example, patients with severe
preeclampsia and a prior myomectomy
would be classified as EB for severe preeclampsia diagnosis even though a history of myomectomy was considered
NEB.

NOVEMBER 2011 American Journal of Obstetrics & Gynecology

456.e2

Research

Obstetrics

A list of diagnoses and their classifications are found in Table 1. Diagnoses considered EB for the late preterm period
included severe preeclampsia/eclampsia,
growth restriction with abnormal fetal
testing (abnormal testing included a biophysical profile of 6/10 or worse, abnormal
umbilical artery or ductus venosus Doppler, or coexisting oligohydramnios), frank
abruption, and a nonreassuring fetal heart
tracing (a category II or III fetal heart
tracing requiring immediate delivery).
Deliveries defined as NEB included stable
patients with the following diagnoses:
chronic hypertension, mild preeclampsia,
gestational hypertension, oligohydramnios (amniotic fluid index 5), intrauterine growth restriction with normal testing,
and prior myomectomy/classic cesarean,
not in labor.
We compared the rate of NICU admission for the 2 groups. At both institutions,
infants are admitted to the NICU based
primarily on morbidity. However, infants
weighing 1800 g (Columbia) and 2200 g
(Christiana) are automatically admitted to
the NICU. There are no other protocolbased admission criteria. To detect the
variable most likely associated with nonweight-based NICU admission, we excluded infants who weighed 1800 and
2200 g, respectively, at either institution.
We also controlled for site (Columbia vs
Christiana), mode of delivery, and gestational age in the multivariable logistic regression model that was created.
Statistical analysis was performed using Stata, Version 10.0 (Stata Corp, College Station, TX). Univariate analysis
was performed using Student t test with
unequal variance, Wilcoxon rank sum,
2, and Fisher exact test when appropriate. A P value of .05 was considered
statistically significant.

R ESULTS
We identified 2756 late preterm pregnancies over the study period. We excluded 9 women with triplets and 54
women who had indeterminate causes of
delivery (Figure). Of the remaining 2693
women, 1429 delivered due to spontaneous labor with intact membranes and
392 delivered for PPROM. Thus, the rate
of nonspontaneous, iatrogenic deliveries
456.e3

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TABLE 2

Indication for delivery and proportion of nonevidence based

Indication for delivery

Total

Nonevidence based

Mild preeclampsia

149

17.1%

31.4%

Oligohydramnios

79

9.1%

16.7%

Gestational hypertension

71

8.1%

15.0%

Elective

61

7.0%

12.9%

Other

55

6.3%

9.6%

Cholestasis

22

2.5%

4.6%

Previa

48

5.5%

4.4%

Myomectomy/prior classic

12

1.4%

2.5%

Chronic hypertension

11

1.3%

2.3%

Prior event

10

1.1%

2.1%

Eclampsia

0.7%

1.3%

Cholelithiasis

0.5%

0.8%

Abnormal testing

30

3.4%

0.2%

Abruption

26

3.0%

0.0%

IUGR

30

3.4%

0.0%

NRFHR

31

3.6%

0.0%

219

25.1%

0.0%

0.9%

0.0%

..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
a
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
b
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................
..............................................................................................................................................................................................................................................

Severe preeclampsia

..............................................................................................................................................................................................................................................

Uterine rupture

..............................................................................................................................................................................................................................................

IUGR, intrauterine growth restriction; NRFHR, nonreassuring fetal heart rate.

a

Composite variable that includes prior intrauterine fetal demise, prior uterine rupture, and prior abruption; b Upon review, testing
was normal.

Gyamfi-Bannerman. Iatrogenic late preterm birth. Am J Obstet Gynecol 2011.

in this late preterm cohort was 32.3%

(n 872/2693). We then categorized
these deliveries by indication and found
that the majority of iatrogenic deliveries,
56.7% (n 494/872), were deemed NEB
(Table 2) for a total of 18.3% (494/2693)
NEB deliveries in the entire late preterm
cohort.
Women in the NEB group were older
(30.0 vs 28.6 years, P .001), more likely
to have twin gestations (18.8% vs 7.9%,
P .001), and more likely to have private insurance (80.3% vs 59.0%, P
.001) (Table 3). The most common NEB
indication for delivery was for mild preeclampsia (31.4%), followed by oligohydramnios (16.7%), and gestational hypertension (15.0%) (Table 2).
The mean gestational age at delivery
was higher in the NEB group (35.7
weeks) compared to the EB group (35.1
weeks, P .001). Also, neonates in the
NEB group were more likely to be delivered in the late preterm period 36

American Journal of Obstetrics & Gynecology NOVEMBER 2011

weeks (70.6% vs 29.4%, P .001). These

infants were also more likely to be
heavier at birth (2665 vs 2306 g, P
.001), and to have an amniocentesis for
fetal lung maturity (8.7% vs 0.8%). In
the univariate analysis, neonates in the
EB group were more likely to be admitted to the NICU (56.0% vs 31.0%, P
.001). After excluding infants admitted
to the NICU for weight criteria and controlling for other confounders, early gestational age (34 vs 36 weeks: odds ratio
[OR], 19.34; 95% confidence interval
[CI], 4.28 87.5) and mode of delivery
(cesarean delivery: OR, 1.88; 95% CI,
1.153.05) were most strongly associated
with NICU admission (Table 4). Babies
delivered at Columbia were less likely to
be admitted to the NICU (OR, 0.38; 95%
CI, 0.19 0.77). Importantly, an EB indication was no longer an independent risk
factor for NICU admission.
There were 54 cases classified as indeterminate. The majority of these cases

Obstetrics

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TABLE 3

Characteristics of evidence-based vs nonevidence-based deliveries

Characteristic

Nonevidence based

Evidence based

P value

Maternal variables

.....................................................................................................................................................................................................................................

Maternal age, y

30

28.6

.001

.....................................................................................................................................................................................................................................

Gravida

2.57

2.64

.54

44.3%

49.3%

.2

0.37

0.39

.59

Prior preterm delivery

15.0%

13.0%

.52

Prior cesarean

78.7%

75.7%

.32

Gestational diabetes

11.2%

9.8%

.52

3.2%

5.3%

.14

.....................................................................................................................................................................................................................................

Nulliparous

.....................................................................................................................................................................................................................................

Abortions

.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................

Pregestational diabetes

.....................................................................................................................................................................................................................................

Twins

18.8%

7.9%

.001

Private insurance

80.3%

59.0%

.001

Tobacco

14.2%

17.8%

Second indication

27.5%

10.1%

.001

5.3

6.5

.001

.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................

.34

.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................

Maternal length of stay, d

..............................................................................................................................................................................................................................................

Neonatal outcomes

.....................................................................................................................................................................................................................................

Gestational age, wk

35.7

35.1

.001

36 wk

70.6%

29.4%

.001

.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................

Birthweight, g

2665

2306.0

.001

.....................................................................................................................................................................................................................................

Apgar 1 (% 8)

54.9%

51.1%

.01

Apgar 5 (% 9)

79.9%

70.3%

.001

Vaginal delivery

43.6%

25.2%

.001

Amniocentesis prior to delivery

8.7%

0.8%

.001

Anomalies

1.4%

1.1%

56.0%

31.0%

.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................
.....................................................................................................................................................................................................................................

.77

.....................................................................................................................................................................................................................................

Infant to NICU

.001

..............................................................................................................................................................................................................................................

NICU, neonatal intensive care unit.

Gyamfi-Bannerman. Iatrogenic late preterm birth. Am J Obstet Gynecol 2011.

(36/54, 66.7%) were because data to support the indication listed could not be
found (eg, severe preeclampsia with normal bloods pressures). The other indications were quite varied, included from
1-4 patients, and included diagnoses such
as vasa previa, neonatal alloimmune
thrombocytopenia, maternal cancers, cerebral infarction, and alcoholic seizures.

C OMMENT
We found that the majority of nonspontaneous late preterm deliveries in our cohort were NEB. Although women with
EB deliveries were more likely to have infants admitted to the NICU, this was not
an independent risk factor for NICU admission in the multivariable analysis,

and the primary factor resulting in NICU

admission was early gestational age.
Overall, 18.3% of our late preterm cohort was delivered for NEB, and potentially avoidable, indications. Our findings demonstrate the need to evaluate
the indications warranting late preterm
delivery, particularly due to the morbidity associated with birth in this gestational age window.
As previously noted, the rate of late
prematurity is increasing steadily in the
United States, and there is concern that
some of these deliveries may not be indicated.5,10 The indications for delivery
vary widely in the late preterm literature.
On one end of the spectrum, Lubow et al
found that only 8% of 149 late preterm

Research

births over 2 years in their institution

were delivered due to nonspontaneous
indications.11 On the other end of the
spectrum, Holland et al10 found that
nearly half of their deliveries were nonspontaneous (46.1%, 237/514).
Traditionally, all preterm deliveries
that are not considered spontaneous
(preterm labor with intact membranes
or PPROM) are designated as indicated12; however, there is an inherent flaw
in this designation. First, the terminology implies that an indicated delivery is
necessary, and second, it does not take
into account different pathophysiologic
mechanisms that lead to indicated preterm birth. Meis and colleagues described risk factors for indicated preterm
birth after defining such deliveries as
nonspontaneous.12 This resulted in 19
varied etiologies of indicated preterm
birth including risk factors such as mullerian abnormalities, race, and chronic
hypertension. While these data are helpful from an epidemiologic perspective,
they do not address pathophysiology or
appropriateness of the indication.
Whether a nonspontaneous preterm
delivery is described as indicated or
elective is subjective. Because there is
an obvious stigma associated with elective preterm delivery, it would be hard to
find elective listed as an indication
for late preterm birth. However, when
Reddy et al,5 reviewed delivery indications for close to 3.5 million births in the
United States in 2001, they found that
23% of late preterm births had no documented indication.10 In their review
they excluded births for obstetric complications, maternal medical conditions,
major congenital abnormalities, and
spontaneous labor without induction or
coexisting obstetrical/medical indications. They speculated that many of these
births without listed indications were
elective due to perceptions of similar
morbidity and mortality risks by either
the patient or the provider. In contrast to
these findings, as previously noted, Holland et al10 found that 10% of those
deliveries were elective. The authors acknowledged that their classification of
the appropriateness of delivery was based
on limited scientific evidence and commented that within their own group,

NOVEMBER 2011 American Journal of Obstetrics & Gynecology

456.e4

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Obstetrics

they debated the appropriateness of each

indication.
It is particularly because of the lack of
consensus regarding accepted indications for preterm delivery and the stigma
associated with elective preterm delivery
that we chose an alternative approach in
designating our deliveries. Although it
could be implied that a NEB delivery is
not indicated, this is far from true. We
simply are saying that there is not
enough evidence to support one practice
over another. Take, for example, timing
of delivery for mild preeclampsia, the
most common NEB diagnosis in our cohort. There are institutional and regional
differences with regard to advocacy for
both late preterm and term delivery of
these pregnancies, yet there are no data
to show improved neonatal outcomes
with either practice. Nor is there evidence to show that maternal outcomes
are improved. A recent clinical trial evaluating labor induction vs expectant
management for mild preeclampsia and
gestational hypertension at 36 weeks
found that maternal outcomes were
improved with labor induction 37
weeks.13 The authors did not find this
trend with delivery between 36-37
weeks, but they cited low numbers in
that subgroup as a reason for further
study at that gestational age. Barton and
colleagues specifically reviewed outcomes with gestational hypertension and
late preterm delivery using a retrospective database.14 They found that elective
delivery from 34-36 weeks resulted in increased neonatal morbidity without maternal benefit. No other clinical trials
have addressed optimal timing of delivery in this setting. The same argument
can be made for our other NEB indications. Oligohydramnios is another diagnosis that commonly leads to iatrogenic
late prematurity, however, the available
literature does not support delivery for
this indication. Zhang et al15 found a
population of women with isolated oligohydramnios and evaluated the correlation with this finding and perinatal
morbidity. Using data from the RADIUS
trial in which women underwent routine
ultrasound screening, they identified a
population of 113 women with isolated
oligohydramnios. There was no associa456.e5

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TABLE 4

Adjusted odds for neonatal intensive care unit admission

Variable

Odds ratio

P value

95% CI

Cesarean
delivery
1.88
.011
1.153.05
..............................................................................................................................................................................................................................................
Evidence
based
0.69
.14
0.431.12
..............................................................................................................................................................................................................................................
Columbia
University
0.38
.007
0.190.77
..............................................................................................................................................................................................................................................
36
wk
1
Referent
..............................................................................................................................................................................................................................................
35
wk
2.91
.001
1.545.48
..............................................................................................................................................................................................................................................
34 wk
19.34
.001
4.2887.5
..............................................................................................................................................................................................................................................

CI, confidence interval.

Gyamfi-Bannerman. Iatrogenic late preterm birth. Am J Obstet Gynecol 2011.

tion with adverse perinatal outcomes in

this group of women. Because the largest
percentage of NEB deliveries was related
to hypertensive disorders of pregnancy
and oligohydramnios, this is where research as to the validity of these indications should be focused.
There are several limitations to this
study. Clearly there are indications for
delivery that are not amenable to an EB
review. For instance, we included uterine
rupture in our list of EB deliveries. We
are not anticipating that a prospective
randomized trial on expectant management of uterine rupture will ever, or
should ever, be attempted. Therefore, as
in the article by Holland et al,10 our designations of NEB vs EB deliveries can be
criticized. Next, we classified twin deliveries as NEB. We did not have information on chorionicity, and there is literature that both supports and refutes
delivery at 37 weeks in the setting of
monochorionic twins.16-18 Finally, we
could not comment on neonatal outcomes beyond NICU admission rates because the neonatal data could not be
linked at 1 of the 2 participating institutions. The strengths of this study are the
large numbers of late preterm deliveries
we were able to evaluate. To our knowledge, this is the largest study looking at
indications for delivery where medical
records were reviewed and diagnoses
were verified. Also, because of institutional variations in practice, we were able
to evaluate a variety of listed indications
rather those only specific to one center.
In conclusion, we found that the majority of nonspontaneous late preterm deliveries in our cohort were NEB. Although
babies from EB deliveries were more likely

American Journal of Obstetrics & Gynecology NOVEMBER 2011

to be admitted to the NICU, this finding

did not hold true after controlling for gestational age at delivery and mode of delivery. Although the individual indication for
delivery likely plays a role, due to the number of indications, we could not reliably
control for these in a logistic regression
model. Regardless, because the majority of
deliveries in this period were NEB, there is
a pressing need to systematically reevaluate
indications for delivery in this period since
data for poorer neonatal outcomes associated with late preterm birth cannot be
refuted.
f
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