You are on page 1of 4

Early Human Development 90 (2014) 5154

Contents lists available at ScienceDirect

Early Human Development


journal homepage: www.elsevier.com/locate/earlhumdev

Effect of placenta previa on neonatal respiratory disorders and amniotic


lamellar body counts at 3638 weeks of gestation
Hiroyuki Tsuda a,, Tomomi Kotani a, Seiji Sumigama a, Yukio Mano a, Li Hua a,b, Hiromi Hayakawa c,
Masahiro Hayakawa d, Yoshiaki Sato d, Fumitaka Kikkawa a
a

Department of Obstetrics and Gynecology, Nagoya University School of Medicine, Nagoya, Japan
Bell Research Center for Reproductive Health and Center, Nagoya, Japan
Department of Obstetrics and Gynecology, Kasugai Municipal Hospital, Kasugai-shi, Aichi, Japan
d
Department of Pediatrics, Nagoya University School of Medicine, Nagoya, Japan
b
c

a r t i c l e

i n f o

Article history:
Received 13 June 2013
Received in revised form 27 September 2013
Accepted 23 October 2013
Keywords:
Amniotic uid
Lamellar body
Placenta previa
Respiratory distress syndrome
Transient tachypnea of the newborn

a b s t r a c t
Background: Pregnancies with placenta previa are signicantly associated with preterm delivery and cesarean
section. Therefore particular attention should be paid to the incidence of neonatal respiratory disorders in
pregnancies with placenta previa.
Aims: The purpose of this study is to examine the relationship between placenta previa and neonatal respiratory
disorders, including respiratory distress syndrome (RDS) and transient tachypnea of the newborn (TTN), and to
evaluate the impact of placenta previa on the amniotic lamellar body count (LBC) values.
Methods: We analyzed the data from 186 registered elective cesarean cases without fetal or maternal complications at 3638 weeks of gestation. Amniotic uid samples were analyzed immediately without centrifugation,
and the LBC was measured using a platelet channel on the Sysmex XE-2100.
Results: RDS was present in four neonates (2.2%) and TTN in 12 neonates (6.5%). The rate of TTN was signicantly
higher and the LBC values were signicantly lower in the placenta previa group than in the control group
(P = 0.002 and P = 0.024). The adjusted odds ratio for neonatal TTN was 7.20 (95% condence interval:
6.587.88) among females with placenta previa. In placenta previa, warning bleeding was a signicant factor
protecting against neonatal respiratory disorders (P = 0.046).
Conclusions: Placenta previa in itself is a risk factor for neonatal TTN. When an elective cesarean section is
performed in cases with uncomplicated placenta previa, special care should be taken to monitor for neonatal
TTN even at 3638 weeks of gestation.
2013 Elsevier Ireland Ltd. All rights reserved.

1. Introduction
The incidence of placenta previa ranges from 3.5 to 4.6 per 1000
births [1]. Patients with placenta previa are more likely to receive
blood transfusions (12% with versus 0.8% without placenta previa)
and to undergo a postpartum hysterectomy, uterine/iliac artery ligation,
or embolization of the pelvic vessels to control bleeding (2.5% with
placenta previa versus 0% without) [2]. Placenta previa increases the
risk of antepartum (RR 9.8), intrapartum (RR 2.5) and postpartum
hemorrhage (RR 1.9) [3]. For these reasons, pregnancies with placenta
previa are signicantly associated with preterm delivery and have a
higher risk for neonatal morbidity and mortality compared to those
without [4]. A retrospective cohort study revealed that the neonatal
mortality rate was 10.7 per 1000 live births when the mothers had
placenta previa compared to 2.5 per 1000 live births in non-previa
Corresponding author at: Department of Obstetrics and Gynecology, Nagoya
University School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya 466-8550, Japan.
Tel.: +81 52 744 2261; fax: +81 52 744 2268.
E-mail address: hiro-t@med.nagoya-u.ac.jp (H. Tsuda).
0378-3782/$ see front matter 2013 Elsevier Ireland Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.earlhumdev.2013.10.005

pregnancies (RR 4.3; 95% CI 4.04.8) [5]. Because of the high rates of
preterm labor and cesarean section in such cases, particular attention
should be paid to the incidence of neonatal respiratory disorders in
pregnancies with placenta previa.
The lamellar body count (LBC) in the amniotic uid is widely
recognized as an accurate predictor of fetal lung maturity [68]. The
LBC can be determined quickly and inexpensively, making it a more
cost-effective predictor of respiratory distress syndrome (RDS) than
the lecithin/sphingomyelin (L/S) ratio [8,9]. Besides RDS, transient
tachypnea of the newborn (TTN) is also a common cause of respiratory
distress during the rst days of life. TTN has been attributed to delayed
absorption of fetal lung uid and in response to increased concentrations of catecholamines and other hormones during labor, the mature
lung epithelium switches from actively secreting chloride and liquid
to actively reabsorbing sodium and liquid [10]. However, evidence has
accumulated that TTN results from mild abnormality of the surfactant
system such as deciency, dysfunction, or both [11,12]. We recently
reported that the LBC in neonates with TTN was signicantly lower
than that in non-RDS/TTN infants [11], therefore we believe that the
pathogenesis of TTN is more likely that of a mild surfactant abnormality

52

H. Tsuda et al. / Early Human Development 90 (2014) 5154

than a delayed absorption of fetal lung uid. The LBC has been reported
to be potentially useful for predicting and distinguishing between RDS
and TTN in singleton pregnancies [11,13].
Previous studies on the neonatal outcome of placenta previa
pregnancies have reported that placenta previa increases the risk for
neonatal RDS [14,15], but these studies were mainly focused on preterm
deliveries. Few studies have focused on this issue in near-term and term
pregnancies. Therefore, in this study, we extracted the pure cesarean
cases without fetal or maternal complications that were delivered at
3638 weeks of gestation, and examined the relationship between
placenta previa and neonatal respiratory disorders, including both RDS
and TTN. Moreover, we measured the amniotic LBC in this study, and
evaluated the impact of placenta previa on the LBC values.

2. Materials and methods


This retrospective study was conducted between September 2009
and November 2012 at Nagoya University Hospital, Nagoya, Japan. All
infants were delivered by scheduled cesarean section at 3638 weeks
of gestation without labor. Cases delivered after 39 weeks of gestation
were excluded because there were no placenta previa cases during
this period. We excluded gestations in which amniotic uid was not
collected, or in which amniotic uid samples were contaminated with
blood and/or meconium. We also excluded all gestations associated
with congenital abnormalities affecting respiratory function, fetal
growth restriction, twin pregnancies, or maternal complications, such
as diabetes mellitus and preeclampsia (Fig. 1). We nally analyzed the
data from 186 registered neonates, including 35 cases with placenta
previa and 151 cases without placenta previa.
All mothers provided written informed consent for this study, which
was approved by the Ethics Committee of Nagoya University Hospital.
The diagnosis of placenta previa was made by ultrasound and MRI. Placenta previa includes both marginal and complete types. Amniotic uid
samples were obtained from the amniotic sac at the time of the cesarean
delivery. Samples were analyzed immediately after arrival at the laboratory, without centrifugation, according to a standardized methodology
for the LBC reported by Neerhof et al. [7]. The LBC was determined
using the platelet channel on an automated hematology analyzer
(Sysmex XE-2100, Sysmex Corporation, Kobe, Japan); the procedure
took less than 30 min. Neonatal data were extracted from the patients'

Uncontaminated Amniotic fluid


samples collected from September
2009 to November 2012 (n=434)

records, including the gestational age at delivery, birth weight, sex,


Apgar scores and respiratory outcomes. Infertility treatment included
articial insemination and in vitro fertilization. Warning bleeding was
dened as painless genital bleeding from the placenta in previa cases.
The diagnoses of RDS and TTN were established by at least two neonatologists based on a combination of clinical signs, the clinical course
and the chest radiography ndings. The clinical criteria for TTN were
presence of tachypnea (respiratory rate N 60 breaths per minute) and
need of supplemental oxygen for at least 6 h. The radiological criteria
for TTN were the presence of perihilar streaking, increased lung
volumes with at diaphragms, mild cardiomegaly, and the presence of
uid in the interlobar ssure and/or pleural space [11]. The neonatologists were blinded to the LBC data.
The data were entered on a computerized spreadsheet (Excel,
Microsoft Japan Co., Ltd., Tokyo, Japan). The Statistical Package for the
Social Sciences (SPSS) software program was used for the data analysis
(V.19.0, SPSS Japan Inc., Tokyo, Japan). The normality of the data was
assessed with the ShapiroWilk test. The MannWhitney U test was
used to compare continuous variables between two groups, with
Student's t-test used as required. The chi-square test was used for the
comparison of categorical variables. Variables which were found to be
signicantly associated with dependent variables at the univariate
level were entered into the multivariate logistic regression model. We
calculated the crude rates of neonatal RDS and/or TTN among patients
with and without placenta previa, and expressed the association
between placenta previa and RDS and/or TTN in term of odds ratios
(ORs) and 95% condence intervals (CIs). Because the rates of neonatal
RDS and/or TTN were low, the odds ratios are fairly accurate representations of the relative risks. Adjusted ORs were derived from logistic
regression models, after controlling for the inuences of gestational
age. A P-value b0.05 was considered to be signicant.
3. Results
3.1. Maternal characteristics
The pregnant females included in this study were separated into two
groups: those with placenta previa and those without (termed controls). The background and characteristics of each group are shown in
Table 1. All infants were delivered by cesarean section without labor.
The maternal age and the ratio of male neonates, neonatal birth weight,
umbilical artery pH and the rate of infertility treatment did not differ
signicantly between the two groups. The gestational age was signicantly lower in previa cases than in control cases (P = 0.002).
3.2. Respiratory outcomes and lamellar body counts
A total of four neonates were diagnosed with RDS (2.2%) and 12
neonates were diagnosed with TTN (6.5%) in this study. The rate of

Exclusion: 248 cases

Table 1
Maternal and fetal characteristics.

Before 36 weeks, 63
After 39 weeks, 33
Twin pregnancy, 52
Fetal growth restriction, 17
Fetal abnormality, 60
Maternal diabetes mellitus, 11
Pregnancy-induced hypertension, 12

Placenta previa
(n=35)

No placenta previa
(n=151)

Fig. 1. The algorithm of the inclusion and exclusion of cases in this study. All infants were
delivered by scheduled cesarean section at 3638 weeks of gestation without labor. In the
gure, contaminated indicates blood and/or meconium.

Maternal age, yearsa,b


Nulliparityc
Male neonatec
GA at delivery, weeksa,b
Neonatal birth weight, ga,d
Apgar score at 5 mina,b
Umbilical artery pHa,b
Infertility treatmentc

Previa
(n = 35)

Control
(n = 151)

P-value

34.2 (3.9)
15/35 (42.9%)
20/35 (57.1%)
37.2 (0.6)
2735 (246)
8.7 (2.1)
7.30 (0.08)
10/35 (28.6%)

33.0 (4.8)
57/151 (37.7%)
73/151 (48.3%)
37.6 (0.6)
2814 (335)
9.3 (0.6)
7.26 (0.60)
24/151 (15.9%)

0.174
0.576
0.348
0.002
0.122
0.089
0.696
0.080

GA, gestational age.


a
Data are presented as the means standard deviation.
b
MannWhitney U test was used.
c
Chi-square test was used.
d
Student t-test was used.

H. Tsuda et al. / Early Human Development 90 (2014) 5154

TTN was signicantly higher in the previa group than in the control
group (20% vs 3.3%; P = 0.002) (Table 2). The LBC values were
signicantly lower in neonates born to mothers with placenta previa
than in control neonates (P = 0.024). The LBC in infants with TTN
(3.60 104/L) was signicantly lower than that in the no RDS/TTN
infants (6.07 104/L) (P = 0.008) (data not shown). In the logistic regression analysis, placenta previa was also a signicant risk factor in the
multivariate model for neonatal TTN after controlling for the maternal
age, gestational age at delivery, neonatal birth weight and infertility
treatment (P = 0.011).
Next, we calculated the OR for neonatal respiratory outcomes
(Table 3), and the risk of neonatal TTN was 7.9-fold greater (OR, 7.86;
95% CI, 2.3226.7) among those with placenta previa. After controlling
for the inuences of gestational age, the neonatal TTN was still 7.2fold greater (adjusted OR, 7.20; 95% CI, 6.587.88, P b 0.001) among
those with placenta previa.
3.3. Age-specic analysis of TTN and LBC
The rate of TTN and LBC at each gestational age (in weeks) is
shown in Table 4. The rate of TTN was signicantly higher, and the
LBC values were signicantly lower, in neonates with previa than
in controls at 37 weeks of gestation (P = 0.007 and P = 0.018). At
36 and 38 weeks of gestation, there were no signicant differences
between the two groups. In the previa group, the LBC value increased
with advancing gestational ages.
3.4. Characteristics of placenta previa cases
We extracted 35 cases of placenta previa and examined the factors
affecting the neonatal respiratory outcomes (Table 5). The gestational
age, sex distribution and umbilical artery pH of the newborn were not
signicantly associated with the occurrence of neonatal respiratory
disorders. The maternal condition, including blood loss during CS and
transfusion, was also not signicantly different between neonates
with and without respiratory disorders. In this study, we did not administer maternal corticosteroid therapy to any of the cases. The cases who
had warning bleeding due to placenta previa signicantly prevented the
occurrence of neonatal respiratory disorders (P = 0.046), and the
infants were free from neonatal RDS/TTN in all cases.
4. Discussion
A high incidence of RDS in neonates born to mothers with placenta
previa has been reported [1416], but many of these reported targeted
preterm delivery, and few studies have focused on term pregnancies.
Therefore, in this study, we extracted the pure cesarean cases without
fetal or maternal complications that were delivered at 3638 weeks of
gestation, and examined the relationship between placenta previa and
neonatal respiratory disorders, including RDS and TTN. Most cases of
TTN are self-limiting, but some cases require nasal continuous positive
airway pressure or mechanical ventilation [17,18], and these neonates

Table 2
Respiratory outcomes and lamellar body counts.

LBC (104/L)a,b
RDSc
TTNc
RDS and TTNc

53

Table 3
Odds ratios for neonatal respiratory outcomes according to the presence of placenta
previa.
Outcome

Odds ratio
(95% CI)

Adjusted odds ratio


(95% CI)

P-value

RDS (n = 4, 2.2%)
TTN (n = 12, 6.5%)
RDS and TTN (n = 16, 8.6%)

1.54 (0.1615.3)
7.86 (2.3226.7)
5.72 (1.9716.7)

0.96 (0.831.12)
7.20 (6.587.88)
4.55 (4.234.89)

0.613
b0.001
b0.001

RDS, respiratory distress syndrome; TTN, transient tachypnea of the newborn; 95% CI, 95%
condence interval.

are prone to asthmatic episodes in the future [19]. A gestational age


younger than 39 weeks was found to be associated with increased risk
for TTN in infants delivered by elective CS [20]. Therefore, physicians
should carefully monitor for neonatal TTN, not only RDS, in infants
born to mothers suffering from placenta previa, because of the high
prevalence of preterm labor and CS.
We have reported that the LBC can predict the occurrence of TTN
[11]. In this study, the rate of TTN was signicantly higher and the LBC
values were signicantly lower in the previa group than in the control
group. The odds ratio of neonatal TTN was 7.20 among females with
placenta previa after controlling for the inuence of gestational age.
Therefore, careful monitoring for neonatal TTN should be performed
for infants born to mothers who had suffered from placenta previa.
This is the rst report about the relationship between placenta previa
and TTN.
We analyzed the age-specic outcome of neonatal TTN based on the
LBC. The rate of TTN was signicantly higher and the LBC values were
signicantly lower in previa cases than in control cases, only at
37 weeks of gestation. Because the risks associated with continuing
the pregnancy (severe bleeding, emergency unscheduled delivery) are
greater than the risks associated with neonatal morbidity after term
pregnancies [21], most obstetricians seem to perform elective CS at
37 weeks of gestation in cases with uncomplicated placenta previa.
Therefore, careful evaluation for neonatal TTN should be performed
even at 37 weeks of gestation. This study provides new and valuable
information about the respiratory outcome in placenta previa.
We evaluated the risk factors for neonatal RDS or TTN in placenta
previa. It has been reported that the risk factors for neonatal RDS are
neonatal asphyxia, maternal bleeding (greater than 500 mL) and no
prenatal steroid administration in cases of placenta previa [22], but we
could not nd any other reports about this issue. In this study, warning
bleeding was the only factor for neonatal RDS or TTN. Glucocorticoids
are known to accelerate fetal lung maturation and reduce the incidence
of RDS. The cortisol levels had been reported to be signicantly lower in
placenta previa cases compared to controls, and this was considered to
be a risk factor for RDS [14]. We speculate that genital bleeding may lead
to stress for the mothers and fetuses in cases with placenta previa,
leading to cortisol production, thus protecting against the occurrence
of neonatal RDS or TTN. Further studies of this issue are necessary to

Table 4
Age-specic analysis of neonatal TTN and lamellar body counts.
Previa

Previa
(n = 35)

Control
(n = 151)

P-value

4.7 (2.6)
1/35 (2.9%)
7/35 (20%)
8/35 (22.9%)

6.1 (3.3)
3/151 (2.0%)
5/151 (3.3%)
8/151 (5.3%)

0.024
0.749
0.002
0.003

LBC, lamellar body count; RDS, respiratory distress syndrome; TTN, transient tachypnea of
the newborn.
a
Data are presented as the means standard deviation.
b
MannWhitney U test was used.
c
Fisher's exact test was used.

The rate of neonatal TTNa


36 weeks
2/7 (28.6%)
37 weeks
4/24 (16.7%)
38 weeks
1/4 (25%)
LBC (104/L)b,c
36 weeks
37 weeks
38 weeks

3.6 (1.8)
4.8 (2.8)
6.8 (2.6)

Control

P-value

3/18 (16.7%)
1/89 (1.1%)
1/44 (2.3%)

0.436
0.007
0.125

7.2 (5.4)
6.4 (2.9)
5.5 (2.8)

0.099
0.018
0.426

TTN, transient tachypnea of the newborn; LBC, lamellar body count.


a
Fisher's exact test was used.
b
Data are presented as the means standard deviation.
c
MannWhitney U test was used.

54

H. Tsuda et al. / Early Human Development 90 (2014) 5154

Conict of interest

Table 5
Characteristics of the placenta previa cases.

Maternal age, yearsa,b


Nulliparityc
Male neonatec
GA at delivery, weeksa,b
Neonatal birth weight, ga,b
Umbilical artery pHa,d
LBC (104/L)a,d
Warning bleedingc
Blood loss during CS, g (range)d
Transfusion of the motherc
Hb one day after CS (g/dL)a,b
Infertility treatmentc

RDS/TTN
(n = 8)

No RDS/TTN
(n = 27)

P-value

32.8 (4.8)
4/8 (50%)
6/8 (75%)
37.0 (0.9)
2829 (193)
7.27 (0.11)
3.6 (3.3)
0/8 (0%)
1529 (3682451)
1/8 (12.5%)
9.52 (1.6)
1/8 (12.5%)

34.7 (3.5)
11/27 (41%)
14/27 (52%)
37.3 (0.5)
2705 (257)
7.31 (0.06)
5.1 (2.3)
10/27 (33%)
1598 (5193193)
11/27 (41%)
9.54 (1.3)
9/27 (33%)

0.225
0.473
0.228
0.509
0.221
0.240
0.157
0.046
0.888
0.146
0.967
0.250

GA, gestational age; LBC, lamellar body count; CS, cesarean section; Hb, hemoglobin; RDS,
respiratory distress syndrome; TTN, transient tachypnea of the newborn.
a
Data are presented as means standard deviation.
b
Student's t-test was used.
c
Fisher's exact test was used.
d
MannWhitney U test was used.

determine whether this is the case. In the placenta previa group, the lack
of difference in LBC has been indicated between the presence and
absence of RDS/TTN. We think that the small number of the cases may
have been the cause of this nding.
Our study has some limitations. First, the gestational age was significantly lower in the previa cases than in the control cases. A lower gestational age can be associated with neonatal respiratory complications.
Therefore, we performed a logistic regression analysis to control for
the inuences of the gestational age, and placenta previa was still a signicant risk factor for neonatal TTN. Placenta previa has been reported
to possibly be associated with respiratory morbidities independent
of gestational age in preterm infants [14,15]. Second, the number of
placenta previa and RDS and/or TTN cases was small. We extracted
the pure cesarean cases after excluding factors which can affect neonatal respiratory outcomes. Therefore, this study exactly reects the relationship between placenta previa and neonatal respiratory outcomes.
This is the strong point of this study. A larger study may be necessary
to overcome the limitations of the present study. Third, the prevention
of neonatal TTN during pregnancy has not been previously demonstrated. We could not prevent neonatal TTN even if we were able to predict
that the neonates were as high risk for having TTN during pregnancy. In
the present circumstances, the management of neonatal TTN relies solely on the neonatal care. Therefore, we recommend delivering the fetuses
whose mothers have placenta previa at tertiary centers where adequate
neonatal care can be given.
In conclusion, this study revealed that the rate of TTN was signicantly higher and the LBC values were signicantly lower in previa cases than
in control cases. According to our analysis of the age-specic outcomes of
neonatal TTN and LBC, only the ndings at 37 weeks of gestation showed
signicant differences. This is the rst report about the relationship between placenta previa and TTN. Placenta previa in itself, as well as factors
such as preterm labor and CS, which have a high prevalence in patients
with placenta previa, are also risk factors for neonatal respiratory disorders. We hope that these data will aid in the management of placenta
previa.

The authors declare that they have no conict of interest.


Acknowledgments
We thank Ms. Sachiko Morisaki for her valuable technical support.

References
[1] Faiz AS, Ananth CV. Etiology and risk factors for placenta previa: an overview
and meta-analysis of observational studies. J Matern Fetal Neonatal Med
2003;13:17590.
[2] Olive EC, Roberts CL, Algert CS, Morris JM. Placenta praevia: maternal morbidity and
place of birth. Aust N Z J Obstet Gynaecol 2005;45:499504.
[3] Crane JMG, Van den Hof MC, Dodds L, Armson BA, Liston R. Maternal complications
with placenta previa. Am J Perinatol 2000;17:1015.
[4] Zlatnik MG, Cheng YW, Norton ME, Thiet MP, Caughey AB. Placenta previa and the
risk of preterm delivery. J Matern Fetal Neonatal Med 2007;20:71923.
[5] Ananth CV, Smulian JC, Vintzileos AM. The effect of placenta previa on neonatal
mortality: a population-based study in the United States, 1989 through 1997. Am J
Obstet Gynecol 2003;188:1299304.
[6] Piazze JJ, Maranghi L, Cerekja A, Meloni P, Gioia S, Fumian L, et al. Amniotic uid lamellar body counts for the determination of fetal lung maturity: an update. J Perinat
Med 2005;33:15660.
[7] Neerhof MG, Haney EI, Silver RK, Ashwood ER, Lee IS, Piazze JJ. Lamellar body counts
compared with traditional phospholipid analysis as an assay for evaluating fetal lung
maturity. Obstet Gynecol 2001;97:3059.
[8] Wijnberger LDE, Huisjes AJM, Voorbij HAM, Franx A, Bruinse HW, Mol BWJ. The
accuracy of lamellar body count and lecithin/sphingomyelin ratio in the prediction
of neonatal respiratory distress syndrome: a meta-analysis. BJOG 2001;108:5838.
[9] Lewis PS, Lauria MR, Dzieczkowski J, Utter GO, Dombrowski MP. Amniotic uid
lamellar body count: cost-effective screening for fetal lung maturity. Obstet Gynecol
1999;93:38791.
[10] O'Brodovich HM. Immature epithelial Na+ channel expressions is one of the pathogenetic mechanisms leading to human neonatal respiratory distress syndrome. Proc
Assoc Am Physicians 1996;108:34555.
[11] Tsuda H, Takahashi Y, Iwagaki S, Uchida Y, Kawabata I, Hayakawa M, et al. Amniotic
lamellar body counts can predict the occurrence of respiratory distress syndrome as
well as transient tachypnea of the newborn (TTN). J Perinat Med 2011;39:24550.
[12] Machado LU, Fiori HH, Baldisserotto M, Ramos Garcia PC, Vieira AC, Fiori RM. Surfactant deciency in transient tachypnea of the newborn. J Pediatr 2011;159:7504.
[13] Tsuda H, Takahashi Y, Iwagaki S, Kawabata I, Hayakawa H, Kotani T, et al. Intraamniotic infection increases amniotic lamellar body count before 34 weeks of
gestation. J Matern Fetal Neonatal Med 2010;23:12306.
[14] Bekku S, Mitsuda N, Ogita K, Suehara N, Fujimura M, Aono T. High incidence of respiratory distress syndrome (RDS) in infants born to mothers with placenta previa. J
Matern Fetal Med 2000;9:1103.
[15] Lin CH, Wang ST, Hsu YC, Lin YJ, Yeh TF, Chang FM. Risk for respiratory distress
syndrome in preterm infants born to mothers complicated by placenta previa.
Early Hum Dev 2001;60:21524.
[16] Crane JMG, Van den Hof MC, Dodds L, Armson A, Liston R. Neonatal outcomes with
placenta previa. Obstet Gynecol 1999;93:5414.
[17] Tudehope DI, Smyth MH. Is transient tachypnea of the newborn always a benign
disease report of 6 babies requiring mechanical ventilation. Aust Paediatr J
1979;15:1605.
[18] Clark RH. The epidemiology of respiratory failure in neonates born at an estimated
gestational age of 34 weeks or more. J Perinatol 2005;25:2517.
[19] Koivisto M, Marttila R, Saarela T, Pokela ML, Valkama AM, Hallman M. Wheezing
illness and re-hospitalization in the rst two years of life after neonatal respiratory
distress syndrome. J Pediatr 2005;147:48692.
[20] Tita AT, Landon MB, Spong CY, Lai Y, Leveno KJ, Varner MW, et al. Timing of elective
repeat cesarean delivery at term and neonatal outcomes. N Engl J Med 2009;360:
U11129.
[21] Spong CY, Mercer BM, D'Alton M, Kilpatrick S, Blackwell S, Saade G. Timing of indicated late-preterm and early-term birth. Obstet Gynecol 2011;118:32333.
[22] Matsuda Y, Ikenoue T, Hokanishi H. The perinatal factors associated with the development of neonatal RDS in cases of placenta previa. Nihon Sanka Fujinka Gakkai
Zasshi 1986;38:9038 [In Japanese].

You might also like