Research ajog.

org

OBSTETRICS
The risk of stillbirth and infant death by each
additional week of expectant management in
twin pregnancies
Jessica M. Page, MD; Rachel A. Pilliod, MD; Jonathan M. Snowden, PhD;
Aaron B. Caughey, MD, PhD

OBJECTIVE: The objective of the study was to compare the fetal/infant
mortality risk associated with each additional week of expectant
management with the mortality risk of immediate delivery in women
with twin gestations.
STUDY DESIGN: A retrospective cohort study was performed utilizing
2006e2008 National linked birth certificate and death certificate
data. The incidence of stillbirth and infant death were determined for
each week of pregnancy from 32 0/7 weeks through 40 6/7 weeks
gestation. Pregnancies complicated by fetal anomalies were excluded.
These measures were combined to estimate the theoretic risk of
remaining pregnant an additional week by adding the risk of stillbirth
during the extra week of pregnancy with the risk of infant death
encountered with delivery during the following week. This composite
fetal/infant mortality risk was compared with the risk of infant death
associated with delivery at the corresponding gestational age.
RESULTS: The risk of stillbirth increased with increasing gestational
age, for example, between 37 and 38 weeks gestation (12.5 per
10,000 vs 22.5 per 10,000; P < .05). As expected, the risk of infant
death following delivery gradually decreased as pregnancies
approached term gestation. Week-by-week differences were statisti-
cally significant (P < .05) between 32 and 36 weeks with decreasing
risk of infant death at advancing gestational ages. The composite risk
of stillbirth and infant death associated with an additional week of
pregnancy had a significant increase from 37 to 38 weeks gestation
(43.9 per 10,000 vs 59.2 per 10,000; P < .05). At 37 weeks
gestation, the relative risk of mortality was statistically significantly
lower with immediate delivery as compared with expectant manage-
ment (relative risk, 0.87; 95% confidence interval, 0.77e0.99).
CONCLUSION: Our results suggest that fetal/infant death risk is
minimized at 37 weeks gestation; however, individual maternal and
fetal characteristics must also be taken into account when determining
the optimal timing of delivery for twin pregnancies.
Key words: expectant management, infant death, stillbirth, twin
pregnancy

Cite this article as: Page JM, Pilliod RA, Snowden JM, et al. The risk of stillbirth and infant death by each additional week of expectant management in twin pregnancies.
Am J Obstet Gynecol 2015;212:630.e1-7.

T win pregnancies are at an increased

risk of stillbirth, antenatal
morbidity, and infant death compared
complications. Maternal comorbidities
such as advanced maternal age, gesta-
tional diabetes, and hypertensive disor-
The risk of stillbirth has also been
shown to vary with gestational age at
delivery in twin pregnancies with an
with singleton gestations.1 This is largely ders are also more common in twin increasing risk at later gestational ages.4-6
due to uteroplacental insufciency, pre- gestations and impart an elevated still- There has been considerable debate
term delivery, and maternal antenatal birth risk.2,3 regarding the contribution of chorio-
nicity to stillbirth risk in uncomplicated
twin gestations. Several studies have
concluded that even in the absence of
From the Department of Obstetrics and Gynecology, University of Utah School of Medicine, Salt Lake monochorionic-specic risks such as
City, UT (Dr Page); Department of Obstetrics and Gynecology, Brigham and Womens Hospital and
twin-twin transfusion syndrome, mon-
Massachusetts General Hospital, Boston, MA (Dr Pilliod); and Department of Obstetrics and
Gynecology, Oregon Health and Science University, Portland, OR (Drs Snowden and Caughey). ochorionic pregnancies experience an
Received Nov. 15, 2014; revised Feb. 11, 2015; accepted March 17, 2015.
increased rate of stillbirth.7,8 Subsequent
work has not demonstrated this phe-
J.M.S. is supported by the Eunice Kennedy Shriver National Institute of Child Health and Human
Development (grant K99 HD079658-01). nomenon, nding more equivalent risks
The authors report no conict of interest.
of stillbirth in monochorionic and
dichorionic pregnancies during the late
Presented in oral format at the 35th annual meeting of the Society for Maternal-Fetal Medicine,
San Diego, CA, Feb. 2-7, 2015. The racing ag logo above indicates that this article was rushed preterm period.4,9-13
to press for the benet of the scientic community. Infant death rates are 5 times higher
Corresponding author: Jessica Page, MD. jessica.page@hsc.utah.edu overall following twin gestations as
0002-9378/$36.00  2015 Elsevier Inc. All rights reserved.  http://dx.doi.org/10.1016/j.ajog.2015.03.033 compared with singleton pregnancies.
Complications of prematurity, congenital

630.e1 American Journal of Obstetrics & Gynecology MAY 2015

ajog.org
anomalies, and low birthweight are the
primary risk factors for infant mortality
in these cases.1 The risk of infant death
varies by gestational age at delivery. Infant
death risk is highest in preterm deliveries
with decreasing incidence as pregnancy
approaches term gestation. The primary
causes of death in these cases have been
shown to be sudden infant death syn-
drome, asphyxia, and sepsis.14-18
The increased risk of both stillbirth
and complications of iatrogenic prema-
turity create a challenging situation
when determining the appropriate
gestational age for delivery, requiring
careful consideration of tradeoffs. Prior
research has suggested that for uncom-
plicated monochorionic and dichorionic
pregnancies, delivery between 36 and 38
weeks gestational age minimizes fetal
and infant mortality.4-6,9,13 Additionally,
a recent Cochrane review concluded that
for uncomplicated twin pregnancies
elective delivery at 37 weeks did not
impart an increased risk of neonatal/in-
fant complications.19 However, the
known complications of late preterm
and early term delivery including respi-
ratory distress syndrome and neonatal
intensive care unit (NICU) admission
must be taken into account when
determining the appropriate gestational
age for delivery.20-28
Given this delicate balance of stillbirth
risk and complications of iatrogenic
prematurity, the decision regarding de-
livery timing for otherwise uncompli-
cated twin pregnancies is challenging.
Using a previously devised composite
measure, we sought to determine the risk
of stillbirth and infant death by week of
gestation in twin pregnancies and to
quantify the risk of expectant manage-
ment vs delivery during the late third
trimester.
M ATERIALS AND M ETHODS
A retrospective cohort study was con-
ducted utilizing 2006-2008 national
linked birth certicate and death certif-
icate data. The National Center for
Health Statistics links live birth cohort
data with infant and fetal death
information.1
We utilized stillbirth data at each
gestational age week and infant death
data following live births at each gesta-
tional age week. Data were investigated
for twin pregnancies from 20 weeks
through 42 weeks gestational age.
Comparisons were made by the indi-
vidual fetus or infant as opposed to the
pair present in each pregnancy. Exclu-
sion criteria included pregnancies
complicated by fetal anomalies.
Additional characteristics of our study
population were also determined
including gestational diabetes, hyper-
tensive disorders, and intrauterine
growth retardation (IUGR). To eliminate
the potential confounding effect these
factors may have on our results
we conducted a secondary analysis
excluding gestational diabetes, hyper-
tensive disorders and IUGR. To better
characterize the morbidity associated
with late preterm and early term de-
liveries, neonatal outcomes by gesta-
tional age including NICU admission,
neonatal seizures, and a need for venti-
lation for greater than 6 hours were
determined.
Our study population included fetal
deaths and live births following delivery
from 32 0/7 through 40 6/7 weeks
gestational age. Pregnancy dating was
determined using the best obstetric es-
timate. This most often refers to the last
menstrual period with an allowance of
the correction of gestational age if the
estimated age based on the last men-
strual period is signicantly different
from that estimated by ultrasound.29
Stillbirth was designated as fetal death
following 20 weeks gestational age. In-
fant death was designated as death
occurring within the rst year of life.
This study was approved by the
Institutional Review Board at Oregon
Health and Science University.
Stillbirth risk was determined using a
fetuses at-risk life table method. This
method accounts for all ongoing fetuses
in the denominator with exclusion of half
the deliveries occurring during the
gestational age week. This technique is
used to reect the fact that a portion of
pregnancies will have delivered at any
given time during the gestational age
week being studied and stillbirths occur
in an even distribution throughout the
week of gestation.30 The calculation
MAY 2015 American Journal of Obstetrics & Gynecology
Obstetrics Research
FIGURE 1
Stillbirth, infant death, and
expectant management risk
calculations
Equation 1 describes the stillbirth risk calcula-
tion, which takes into account fetuses at risk by
dividing the number of stillbirths by all ongoing
fetuses minus half the deliveries occurring at the
gestational age week studied. Equation 2
displays the infant death calculation with the
number of infant deaths divided by the total
number of live births at that gestational age.
Equation 3 shows the composite risk associated
with expectant management with the stillbirth
risk during the additional week of expectant
management added to the infant death risk
following delivery at the subsequent week.
GA, gestational age.
Page. Fetal/infant mortality risk in twin pregnancies by
gestational age at delivery. Am J Obstet Gynecol 2015.
includes the number of stillbirths occur-
ring at a given gestational age in the
numerator divided by the fetuses at-risk
as described above (Figure 1, equation 1).
Infant death risk was calculated by
dividing the number of infant deaths by
the number of live births at the corre-
sponding gestational age (Figure 1,
equation 2). To estimate the risk of fetal/
infant mortality associated with each
additional week of pregnancy, a com-
posite risk was calculated. This calcula-
tion included the risk of stillbirth
associated with the additional week of
pregnancy in addition to the risk of in-
fant death following the gestational age
at delivery (Figure 1, equation 3).
Stillbirth, infant death, and composite
fetal/infant mortality risks were deter-
mined for each week of gestation in twin
pregnancies from 32 0/7 through 40 6/7
weeks gestational age. This period was
chosen because of the prevalence of
preterm and early term delivery in this
population with rare occurrence of de-
livery past 40 weeks gestation. Stata
software (version 11; Stata Corp, College
630.e2
Research Obstetrics ajog.org

Station, TX) was used to perform the c2

analysis of fetal infant mortality at each TABLE 1
gestational age. Risk of fetal/infant death per 10,000 twins
To determine the optimal gestational Fetal/infant death
age for delivery, the composite risk of per additional week
IUFD per 10,000 Infant death per expectant management
expectant management for an additional
GA fetuses (95% CI) 10,000 births (95% CI) (95% CI)
week of pregnancy was compared with
the risk of infant death for each gesta- 32 6.2 (2.8e9.5) 133.2 (117.7e148.8) 101.2 (92.4e110.0)
tional age week during this period. This 33 5.0 (2.4e7.6) 95.0 (83.8e106.3) 80.3 (74.0e86.6)
method accounts for the infant mortality 34 7.1 (4.7e9.4) 75.3 (67.6e83.0) 58.8 (54.4e63.2)
associated with earlier delivery vs the
35 7.0 (5.1e9.0) 51.7 (46.4e57.1) 49.3 (45.9e52.7)
additional risk of stillbirth during the
extra week of pregnancy and the corre- 36 9.8 (7.8e11.8) 42.2 (38.1e46.4) 47.8 (44.7e50.8)
sponding infant death risk following 37 12.5 (10.3e14.7) 37.9 (34.2e41.7) 43.9 (40.7e47.0)
delivery at the next week of gestation. 38 22.5 (18.9e26.0) 31.4 (27.2e35.6) 59.2 (54.0e64.3)
Fetal/infant mortality risk was calcu-
39 23.4 (16.2e30.6) 36.7 (27.7e45.7) 75.4 (64.2e86.5)
lated per 10,000 fetuses at risk/live
births. Stillbirth, infant death, and 40 69.2 (47.9e90.6) 52.0 (33.4e70.5) 190.9 (157.1e224.7)
composite fetal/infant mortality data are CI, confidence interval; GA, gestational age; IUFD, intrauterine fetal death.
displayed in table format to facilitate Page. Fetal/infant mortality risk in twin pregnancies by gestational age at delivery. Am J Obstet Gynecol 2015.
comparison of each value by gestational
age. The risks of infant death and com-
posite mortality were graphed to display
the gestational age at which overall fetal/ only between 37 and 38 weeks gestation The relative risk of fetal/infant mor-
infant mortality risk is minimized. (12.5 per 10,000 vs 22.5 per 10,000) and tality of delivery vs expectant manage-
We calculated the relative risk of between 39 and 40 weeks gestation (23.4 ment was calculated for gestational ages
stillbirth and infant death incurred by an per 10,000 vs 69.2 per 10,000). Infant from 32 through 40 weeks gestation
additional week of pregnancy compared death risk was highest at early gestational (Table 2). We found an increased risk of
with the risk of infant death following ages, decreasing as gestational age mortality associated with delivery at 34
delivery at the gestational age in ques- approached term (Table 1). The infant weeks compared with expectant man-
tion. The 95% condence interval for death risk nadir was found at 38 weeks agement, with a statistically signicant
the relative risks were calculated and gestation (31.4 per 10,000). relative risk 1.28 (95% condence in-
deemed to be statistically signicant if The composite fetal/infant death risk terval [CI], 1.15e1.44). The relative
they did not contain 1. from expectant management for 1 week risks at 35 and 36 weeks gestation were
A number needed to treat analysis was was minimized at 37 weeks gestation not statistically signicant. At 37 weeks,
also performed to determine the number (Table 1). Risks were highest at the ex- the risk prole favored delivery as
needed to deliver by a given gestational tremes of the gestational ages studied. opposed to continued expectant man-
age to avoid 1 fetal/infant death during Increased infant death risk imparted agement with a relative risk 0.87 (95%
the additional week of pregnancy. This higher mortality rates in early gestational CI, 0.77e0.99). Delivery continued to be
calculation was performed by deter- ages; conversely, elevated stillbirth risk the preferred management at advancing
mining the inverse of the difference be- was reected at later gestational ages. gestational ages with decreasing relative
tween the mortality probability of the The highest fetal/infant mortality risk risks associated with delivery as dis-
expectant management and infant death from expectant management was played in Table 2.
at each gestational age week. observed at 40 weeks gestation (190.9 A number needed to deliver to avoid 1
per 10,000). When comparing the rate of fetal/infant death by gestational age was
R ESULTS mortality from immediate delivery (in- also determined (Table 3). With
A total of 454,626 twins was included in fant death) with that of expectant man- advancing gestational age, the number
our analysis of twin gestations with still- agement for 1 week, the rate was needed to deliver decreased, reecting
birth or live birth occurring from 32 0/7 statistically signicantly higher for im- the increased stillbirth risk at later
through 40 6/7 weeks gestational age. mediate delivery from 32 to 34 weeks gestational ages. For example, there
Stillbirth was observed in 1585 fetuses gestation (Figure 2). From 35 to 36 would be 1689 deliveries needed at 37
(0.35%) and infant death following 2357 weeks gestation, there was no statisti- weeks gestation to prevent 1 death as
live births (0.52%) overall. The risk of cally signicant difference (Table 1). compared with 360 deliveries needed at
stillbirth increased with each additional From 37 weeks gestation and onward, 38 weeks gestation to prevent 1 death.
week of pregnancy (Table 1). However, the mortality risk was greater with An additional analysis of our data
this increase was statistically signicant expectant management. excluding those pregnancies complicated

630.e3 American Journal of Obstetrics & Gynecology MAY 2015

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FIGURE 2 TABLE 2
Risk of fetal/infant death per week of expectant management vs delivery Relative risk of fetal/infant
in 10,000 twins mortality with each additional
week of expectant management
vs delivery
GA RR 95% CI
34 1.28 (1.15e1.44)
35 1.05 (0.94e1.18)
36 0.88 (0.79e1.00)
37 0.87 (0.77e0.99)
38 0.53 (0.45e0.63)
39 0.49 (0.36e0.67)
40 0.27 (0.18e0.43)
CI, confidence interval; GA, gestational age; RR, relative
risk.
Page. Fetal/infant mortality risk in twin pregnancies
by gestational age at delivery. Am J Obstet Gynecol
2015.

The risk of infant death following delivery and composite fetal/infant mortality risk with expectant
management are shown by gestational age in twin pregnancies from 32 through 40 weeks
gestation.
Page. Fetal/infant mortality risk in twin pregnancies by gestational age at delivery. Am J Obstet Gynecol 2015.
by gestational diabetes, hypertensive
disorders, and IUGR was performed to
ascertain the comparison in a low-risk
twin cohort. Table 4 displays the ratio
of stillbirths, rate of infant death, and
composite risk estimate by gestational
age in this group. Figure 3 displays the
rate of infant death vs mortality risk of
expectant management. This compares
the mortality risk of immediate delivery
vs continued pregnancy for 1 additional
week. The result was similar with that
found in our primary study group, but
now 38 weeks gestation is when a sta-
tistically signicantly lower mortality
rate is produced by delivery as compared
with expectant management.
Analysis of neonatal complications
by gestational age at delivery is shown
in Table 5. The NICU admission rate
was lowest following delivery at 38
weeks gestation, and the NICU admis-
sion rate decreased signicantly with
each additional week of pregnancy from
32 through 38 weeks gestational age.
Additional outcomes studied included
neonatal seizures and a need for me-
chanical ventilation. Because of the low
poorly identied, the 37 vs 38 week issue is
not fully answered by this analysis in
which most SGA/IUGR was identied by
birthweight.
Even with these analyses, the decision
incidence of seizures, there were no sig- between delivery at 37 vs 38 weeks is
nicant differences found by gestational unclear. Although the risk of stillbirth
age at delivery. The need for ventilation would be reduced by delivery at 37
for greater than 6 hours of time was used weeks, the risk of complications of pre-
as a marker for neonatal respiratory maturity with subsequent increased
complications. Signicantly fewer cases likelihood of infant death at this
of mechanical ventilation were found
with advancing gestational age from
32 through 38 weeks.
TABLE 3
C OMMENT Number needed to deliver to
Our work demonstrates that the risk of prevent 1 fetal/infant death in
immediate delivery is lower than the additional week of expectant
expectant management at 37 weeks management
gestation for unselected twin pregnan- GA NNT
cies in the absence of fetal anomalies. 34 606
This corresponds with prior studies that 35 4071
have also recommended this timing of
delivery for uncomplicated dichorionic 36 1811
pregnancies.4,9,13 37 1689
When limited to the lower-risk twin 38 360
pregnancies, excluding gestational dia-
39 259
betes, hypertension, and small-for-
gestational-age (SGA)/IUGR pregnancies, 40 72
38 weeks became the threshold above GA, gestational age; NNT, number needed to treat.
which mortality only increased. Although Page. Fetal/infant mortality risk in twin pregnancies
by gestational age at delivery. Am J Obstet Gynecol
this analysis suggests 38 weeks in the 2015.
lowest-risk group because SGA/IUGR is so

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monochorionic twins toward the end of

TABLE 4 the third trimester and the relative risk of
Risk of fetal/infant death per 10,000 twins excluding those complicated stillbirth between the 2 subgroups of
by GDM, HTN, and IUGR twins. Among twins beyond 34 weeks
Fetal/infant death gestation, approximately 10% are mon-
per additional week ochorionic and the relative risk of still-
IUFD per 10,000 Infant death per expectant management
birth is 1.69 (95% CI, 1.04e2.75).5,31
GA fetuses (95% CI) 10,000 births (95% CI) (95% CI)
Given these estimates, this suggests that
32 5.1 (1.6e8.5) 102.1 (86.6e117.6) 81.8 (72.0e91.6) our estimate of fetal death for twins is
33 3.9 (1.2e6.5) 76.8 (65.0e88.5) 64.3 (56.7e71.9) approximately 7% above the actual risk
34 5.0 (2.7e7.4) 60.4 (52.3e68.6) 43.6 (38.7e48.5) for dichorionic twins.
Additionally, with such administrative
35 4.4 (2.5e6.3) 38.5 (32.9e44.2) 38.2 (34.2e42.1)
data, there is often a concern of under-
36 7.5 (5.3e9.6) 33.8 (29.2e38.4) 35.4 (32.1e38.7) coding of outcomes. However, because
37 6.7 (4.7e8.7) 27.9 (23.9e32.0) 25.8 (23.0e28.5) these data are generated by linking birth
38 17.3 (13.0e21.5) 19.0 (14.6e23.5) 47.0 (42.0e51.9) and death certicates, the chances of
undercoding of mortality are relatively
39 14.0 (5.5e22.6) 29.7 (17.3e42.1) 46.8 (35.8e57.8)
small. We chose to study stillbirth and
40 46.6 (15.5e77.7) 32.7 (6.6e58.9) 193.7 (149.1e238.2) infant death as our primary outcomes,
CI, confidence interval; GA, gestational age; GDM, gestational diabetes; HTN, hypertensive disorders; IUFD, intrauterine fetal given that they are well coded in
death; IUGR, intrauterine growth restriction.
administrative data (death certicates),
Page. Fetal/infant mortality risk in twin pregnancies by gestational age at delivery. Am J Obstet Gynecol 2015.
of clinical importance, and are rare oc-
currences that are best studied using
large databases such as that utilized here.
gestational age is higher as compared risk of stillbirth in uncomplicated Our composite risk of expectant man-
with 38 weeks. However, common ob- monochorionic vs dichorionic preg- agement is intended to be an estimate of
stetric practice entails individualized nancies. Although some have found an overall mortality risk by week of gestation,
counseling regarding risk factors, cir- increased risk of stillbirth independent which is multifactorial and inuenced by
cumstances, and patient preferences, of typical risk factors associated with maternal and neonatal factors. Some of
and this increased risk of stillbirth is monochorionicity such as twin-twin these factors are independent of gesta-
often unacceptable to a patient in com- transfusion, others have not repro- tional age, but others have been shown to
parison with the risk of possible infant duced this risk.7,8 We did not have vary by gestational age.20,32
mortality and neonatal complications. information on the complication of Given the lack of detail regarding
Given that our analysis was conducted twin-to-twin transfusion syndrome. chorionicity in our work, it is difcult to
with fetus level data as opposed to This complication would bias the results make specic conclusions regarding the
pregnancy level data, the risk of both toward higher rates of stillbirth. How- ideal gestational age for delivery. How-
stillbirth and of infant death is essentially ever, given the low incidence of this ever, our work does seem to correlate
double the risks we have estimated in disorder in the late preterm and term with prior recommendations with
Table 1 because the event could occur to periods, this would likely be only a very decreasing mortality risk around 37
1 twin or the other. This fact is relevant small source of bias in the study. weeks gestation for both mono-
in patient counseling because the Several studies have estimated a chorionic and dichorionic pregnancies.
expectant mother is carrying 2 fetuses at similar risk of stillbirth at gestational These guidelines include consideration
risk. ages longer than 32 weeks between un- of expectant management for mono-
Whereas this study is the rst to complicated monochorionic and chorionic pregnancies through 37 6/7
compare the long-term impact of im- dichorionic pregnancies.10-13 Given the weeks gestation and dichorionic preg-
mediate delivery, infant death, with variation in the recommended timing of nancies through 38 6/7 weeks.33,34
expectant management in twins, it is not delivery and stillbirth risk for mono- Given that most pregnancies
without limitations. This work is based chorionic and dichorionic pregnancies, continuing to 38 weeks and beyond are
on birth certicate data and as such is this represents a considerable limitation likely dichorionic, this may reect an
limited by the coding and accuracy of in our work and an important area of increased rate of stillbirth warranting
data available. Because of these date, future research. delivery by 38 weeks gestation for
detailed information regarding chorio- To estimate how the combination of dichorionic pregnancies. However, be-
nicity is not available, which would be an monochorionic and dichorionic twins cause we cannot examine dichorionic
important analysis to perform. would have an impact on the mortality pregnancies specically in this study,
Several studies have examined the ef- risks near and at term, one needs to be further work is needed to better clarify
fect of chorionicity on the prospective able to estimate the prevalence of this potential risk. It is also notable that

630.e5 American Journal of Obstetrics & Gynecology MAY 2015

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complications that may indicate earlier
FIGURE 3 delivery. -
Risk of fetal/infant death excluding GDM, HTN, and IUGR

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