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Epidemiology

DOI: 10.1111/1471-0528.12444
www.bjog.org

Risk of retained placenta in women previously


delivered by caesarean section: a
population-based cohort study
J Belachew,a S Cnattingius,b A Mulic-Lutvica,a K Eurenius,a O Axelsson,a,c AK Wikstroma,b
a

Department of Womens and Childrens Health, Uppsala University, Uppsala, Sweden b Clinical Epidemiology Unit, Department of
Medicine, Karolinska Institute, Solna, Sweden c Centre for Clinical Research Sormland, Uppsala University, Uppsala, Sweden
Correspondence: Dr J Belachew, Department of Womens and Childrens Health, Uppsala University, SE-75185 Uppsala, Sweden.
Email johanna.belachew@kbh.uu.se
Accepted 26 July 2013. Published Online 16 September 2013.

Objective To evaluate whether women with a caesarean section at

Main outcome measures Retained placenta with normal

their first delivery have an increased risk of retained placenta at


their second delivery.

(1000 ml) and heavy (>1000 ml) bleeding.

deliveries in Sweden during the years 19942006 (n = 258 608).


Women with caesarean section or placental abruption in their
second pregnancy were not included in the study population.

Results The overall rate of retained placenta was 2.07%. In women


with a previous caesarean section and in women with previous
vaginal delivery, the corresponding rates were 3.44% and 1.96%,
respectively. Compared with women with a previous vaginal
delivery, women with a previous caesarean section had an increased
risk of retained placenta (adjusted OR 1.45; 95% CI 1.321.59), and
the association was more pronounced for retained placenta with
heavy bleeding (adjusted OR 1.61; 95% CI 1.441.79).

Methods The risk of retained placenta at second delivery was

Conclusions Our report shows an increased risk for retained

estimated for women with a first delivery by caesarean section


(n = 19 458), using women with a first vaginal delivery as
reference (n = 239 150). Risks were calculated as odds ratios by
unconditional logistic regression analysis with 95% confidence
intervals (95%) after adjustments for maternal, delivery, and
infant characteristics.

placenta in women previously delivered by caesarean section, a


finding that should be considered in discussions of mode of
delivery.

Design Population-based cohort study.


Setting Sweden.
Population All women with their first and second singleton

Keywords Caesarean section, postpartum hemorrhage, retained

placenta.

Please cite this paper as: Belachew J, Cnattingius S, Mulic-Lutvica A, Eurenius K, Axelsson O, Wikstrom AK. Risk of retained placenta in women previously
delivered by caesarean section: a population-based cohort study. BJOG 2014;121:224229.

Introduction
The increasing rate of caesarean sections worldwide has
been a major concern reported in the obstetric scientific literature of the last few years. In the USA as well as in Australia the rate has reached nearly 30%, which is well above
the WHO recommendation of 15%.13 As a consequence of
this increasing rate, delivery complications related to previous caesarean sections, such as placenta praevia, placenta
accreta, and uterine rupture, have increased.4
Retained placenta after vaginal delivery is a potentially
life-threatening complication because of its strong association with postpartum haemorrhage. Following uterine
atony it is the second most common cause of postpartum

224

haemorrhage and the most common indication for blood


transfusion postpartum.5 Manual removal of the retained
placenta has also been shown to increase the risk of postpartum endometritis.6 In the UK and Ireland the rate of
retained placenta has increased during the last century.7
The importance of identifying risk factors for retained
placenta is highlighted in many studies. High maternal age,
preterm labour, and a previous history of retained placenta
are factors known to increase the risk at forthcoming deliveries.811 Another potential risk factor for retained placenta
is a previous caesarean section; however, results from earlier studies are contradictory. Some studies have shown
that a previous caesarean section increases the risk for
retained placenta,12,13 whereas others show no

2013 Royal College of Obstetricians and Gynaecologists

Retained placenta and previous caesarean section

increase.10,11,14 These previous studies have not distinguished between retained placenta with normal versus
heavy bleeding.
In the present nationwide Swedish study, we included
more than 250 000 women with their first and second
deliveries between 1994 and 2006. The aim was to investigate whether women with a caesarean delivery at their first
delivery have an increased risk of retained placenta at their
second delivery.

Methods
The Swedish Medical Birth Register is a large national
population-based database, established in 1973. It includes
information on more than 98% of all births in Sweden,
such as demographic data, reproductive history, pregnancy
complications, and delivery and neonatal characteristics.15
In Sweden antenatal care is standardised and free of charge.
During the first antenatal visit, usually taking place at the
end of the first trimester, the mother is interviewed about
her medical and reproductive history and smoking habits.16
The mothers height and weight are recorded. Complications during pregnancy and delivery are classified according
to the International Classification of Diseases (ICD), as
noted by the responsible doctor. The ninth version of the
ICD (ICD-9) was used for the period 19941996, and
thereafter the tenth version was used (ICD-10). Information on each pregnancy and delivery is forwarded to the
birth register through copies of standardised antenatal,
obstetric, and paediatric records. Individual record linkage
between the birth register and other registers is possible
through each individuals unique personal registration
number, assigned to each Swedish resident.17

Study population
During the years 19942006 approximately 1.3 million
births were recorded in the birth register. During this period, 296 251 women had their first and second consecutive
singleton pregnancies resulting in birth at 22 weeks of gestation or later. We excluded 37 643 women who had a caesarean section or a placental abruption in their second
pregnancy, as retained placenta is not a possible outcome
for these women. The final study population included
258 608 women.

Exposure
Exposure was defined as a first delivery by caesarean section.
The mode of delivery (caesarean, vaginal instrumental, or
vaginal spontaneous) is recorded in the birth register.

Outcome
The outcome examined was a second vaginal delivery complicated by retained placenta. In Sweden, the recommended

2013 Royal College of Obstetricians and Gynaecologists

clinical practice is to perform manual removal of the placenta 3060 minutes after delivery of the child according
to the National Institute of Health and Clinical Excellence
(NICE) guidelines in the UK.18 Retained placenta was identified by the ICD-9 codes 666A and 667A, and by the
ICD-10 codes O720 and O730. Retained placenta with
normal (1000 ml) as opposed to heavy (>1000 ml) bleeding was ascertained by separating ICD-9 code 667A and
ICD-10 code O730 (normal bleeding) from ICD-9 code
666A and ICD-10 code O720 (heavy bleeding).

Covariates
We considered maternal reproductive history, sociodemographic, and anthropometric characteristics, as well as delivery and infant characteristics as possible confounding
factors. Information on maternal body mass index (BMI),
height, smoking habits, cohabitation with the infants father,
number of previous miscarriages and in vitro fertilisation in
the present pregnancy was collected from the first antenatal
visit in the second pregnancy. We did not have access to
data on previous terminations of pregnancy. At delivery,
information on maternal age, premature rupture of membranes (ICD9 code 658B and ICD-10 code O42), labour
dystocia (ICD-9 code 661 and ICD-10 code O62), mode of
delivery (vaginal instrumental or vaginal non-instrumental
delivery), as well as gestational length, infant birthweight,
and infant sex was collected. In Sweden, gestational age is
assessed by ultrasound scans in 97% of pregnant women,
usually in the early second trimester.19 If no information
about ultrasound was available, gestational age was calculated from the last menstrual period. Information on the
mothers educational level was obtained from the education
registry from 2005. The Registry of Population and Population Changes provided information on the mothers country
of birth. The interpregnancy interval was calculated as the
number of years between the birth of the first child and the
estimated date of conception of the second child. All variables were categorised according to Table 1.

Statistics
The risk of retained placenta at second delivery was estimated for women with a first delivery by caesarean section,
using women with a first vaginal delivery as reference. Risks
were calculated as odds ratios by unconditional logistic
regression analysis with 95% confidence intervals. Maternal
characteristics, including age, height, smoking habits, country of birth, previous miscarriages, in vitro fertilisation,
years of interpregnancy interval, maternal BMI, cohabitation with the infants father, and years of formal education
were recognised as possible confounding factors. The last
three variables were not associated with our outcome in
univariate analyses, and were therefore excluded from
further analyses. In a first multiple logistic model, we calcu-

225

Belachew et al.

Table 1. Rates and risk of retained placenta according to maternal,


delivery, and infant characteristics at second delivery
Number
of births

Rate (%)

Maternal characteristics
Maternal age (years)
<25
31 091
2529
91 166
3034
100 040
35
36 311
Maternal height (cm)
<162
70 906
162171
126 619
172
42 867
Missing
18 216
Body mass index
second birth
<18.5
5213
18.524.9
142 574
25.029.9
55 500
30.0
20 945
Missing
34 376
Smoking
Yes
19 087
No
222 421
Missing
18 669
Living with the father for second
Yes
238 544
No
5474
Missing
14 590
Education (years)
12
61 131
>12
171 646
Missing
25 831
Mothers country of birth
Nordic
225 840
Non-Nordic
31 642
Missing
1126
Previous miscarriages (numbers)
0
206 339
12
49 479
3
2790
In vitro fertilisation
Yes
2056
No
256 552
Interpregnancy interval (years)
<1
Data missing
47 962
13
183 350
46
22 071
7
4763

0.81 (0.730.90)
Ref.
1.28 (1.201.36)
1.59 (1.471.72)

1.85
2.06
2.41

0.90 (0.840.96)
Ref.
1.17 (1.091.26)

0.97 (0.791.18)
Ref.
1.03 (0.971.11)
1.07 (0.971.18)

2.37
2.03

1.18 (1.061.30)
Ref.

birth
2.05
2.12

1.03 (0.861.24)
Ref.

2.17
2.12

1.03 (0.961.09)
Ref.

2.13
1.68

Ref.
0.79 (0.720.86)

1.92
2.62
3.48

Ref.
1.38 (1.291.47)
1.84 (1.502.26)

3.36
2.06

1.65 (1.302.10)
Ref.

1.98
2.04
2.32
2.88

0.97 (0.911.04)
Ref.
1.14 (1.041.26)
1.42 (1.201.69)

Rate (%)

Delivery and infant characteristics


Premature rupture of membranes
Yes
2046
4.89
No
256 562
2.05
Induction of labour
Yes
20 138
3.45
No
236 439
1.96
Missing
2031
Labour dystocia
Yes
14 266
3.29
No
244 342
2.00
Instrumental vaginal delivery
Yes
9180
3.37
No
249 428
2.02
Epidural
Yes
46 017
2.77
No
212 591
1.92
Gestational length (weeks)
31
603
9.45
3236
6913
3.79
3741
217 898
1.92
42
32 868
2.53
Missing
326
Infant birthweight (g)
<2000
907
7.83
20002999
19 994
2.56
30003999
174 082
1.86
40004999
61 418
2.38
5000
1419
3.66
Missing
788
Infant sex
Boy
132 723
1.89
Girl
125 885
2.25
Total births
258 608
2.07

Crude OR (95% CI)

2.46 (2.013.01)
Ref.
1.79 (1.651.94)
Ref.

1.67 (1.521.84)
Ref.
1.69 (1.501.90)
Ref.
1.46 (1.371.56)
Ref.
5.33 (4.057.01)
2.01 (1.772.28)
Ref.
1.33 (1.231.43)

4.48 (3.505.72)
1.39 (1.261.52)
Ref.
1.29 (1.211.37)
2.01 (1.522.65)

Ref.
1.19 (1.131.26)

CI, confidence interval.

lated risk of retained placenta related to maternal characteristics, and risks were adjusted for the remaining maternal
characteristics and for year of second delivery (with the latter categorised into 19941997, 19982002, and 20032006).

226

Number
of births

Crude OR (95% CI)

1.44
1.78
2.27
2.79

1.98
2.04
2.11
2.18

Table 1. (Continued)

Thereafter we created a second multiple logistic model by


adding delivery and infant characteristics, such as prelabour
rupture of membranes, induction of labour, labour dystocia,
instrumental vaginal delivery, use of epidural anaesthesia,
gestational length at delivery, infant birthweight, and infant
sex. Maternal, delivery, and infant characteristics were categorised according to Table 1. All analyses were performed
using SAS 9.1 (SAS Institute Inc., Cary, NC, USA), and all
variables adjusted for were independently statistically associated with our outcome at the level of 5%.

Results
In this population, 2.07% of the women were diagnosed
with retained placenta. Table 1 presents risk of retained

2013 Royal College of Obstetricians and Gynaecologists

Retained placenta and previous caesarean section

placenta according to maternal, delivery, and infant characteristics. Older and taller mothers had increased risks compared with younger and shorter women. Women born
outside the Nordic countries had a decreased risk compared with Nordic women. Smoking, previous miscarriages,
and in vitro fertilisation increased the risk of retained placenta. Delivery characteristics, including prelabour rupture
of membranes, induction of labour, labour dystocia, instrumental vaginal delivery, and epidural use increased the risk
for retained placenta. The highest OR values for retained
placenta were shown for preterm delivery and low infant
birthweight. Maternal BMI, cohabitation with the infants
father, and years of formal education had no impact on the
outcome (Table 1).
Compared with women who had a vaginal first delivery,
women with a caesarean first delivery had a crude OR of
retained placenta at their second delivery of 1.79 (95% CI
1.651.94; Table 2). Adjustments for maternal characteris-

tics had only a minor affect on this association. Adjustments


for delivery and infant characteristics from the second delivery attenuated the risk to some extent (Table 2). When
separate analyses were made for retained placenta with normal compared with heavy bleeding, a previous caesarean
delivery was only associated with retained placenta and
heavy bleeding (adjusted OR 1.61; 95% CI 1.651.94;
Table 3).
In Table S1 the adjusted risks of retained placenta in second delivery are presented for all maternal, delivery, and
infant characteristics presented in Tables 1 and 2. The
highest adjusted odds ratio for retained placenta was seen
for preterm delivery (<32 weeks of gestation): OR 3.31
(95% CI 2.025.42). The risk of retained placenta after a
first delivery with caesarean section was at a similar level as
in pregnancies with a mother of high age (35 years), three
or more prior miscarriages, induced labour, and in deliveries of small (<2000 g) or large (5000 g) infants.

Table 2. Rates and risk of retained placenta at second delivery, by caesarean section at first delivery
Caesarean section
at first delivery

Total numbers

Retained placenta at second delivery


No.

No
Yes

239 150
19 458

4680
670

Rates (%)

1.96
3.44

OR (95% CI)
Crude OR

Adjusted OR model 1

Adjusted OR model 2

Ref.
1.79 (1.651.94)

Ref.
1.75 (1.611.91)

Ref.
1.45 (1.321.59)

A total of 37 643 women with caesarean section or placental abruption in the second delivery were excluded from the study population.
Model 1 was adjusted for: maternal age; height; smoking; country of birth; previous miscarriage; in vitro fertilisation; and years of interpregnancy
interval.
In addition to the confounding factors listed in model 1, model 2 adjusted for: premature rupture of membranes; induction of labour; dystocia;
vacuum extraction; epidural use; gestational length, infants weight, infants sex and year of second birth.

Table 3. Rates and risks of retained placenta with heavy (>1000 ml) or normal (1000 ml) bleeding at second delivery, by caesarean section at
first delivery
Caesarean section
at first delivery

No
Yes

Retained placenta second delivery

No.

Rates (%)

3294
493

1.4
2.5

Heavy bleeding

Normal bleeding

OR (95% CI)

OR (95% CI)

Crude OR

Adjusted OR*

No.

Rates (%)

Ref.
1.87 (1.702.06)

Ref.
1.61 (1.441.79)

1386
177

0.6
0.9

Crude OR

Adjusted OR*

Ref.
1.59 (1.361.87)

Ref.
1.11 (0.921.33)

CI, confidence interval.


A total of 37 643 women with placental abruption or caesarean section at second delivery were excluded from the study population.
*Adjusted for: maternal age; height; smoking; country of birth; previous miscarriage; in vitro fertilisation; interpregnancy interval (years); and year
of second birth. At second birth: premature rupture of membranes; induction of labour; dystocia; vacuum extraction; epidural use; gestational
length; infant weight; and infant sex.

2013 Royal College of Obstetricians and Gynaecologists

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Belachew et al.

Discussion
Main findings
In this large population-based cohort study of women with
both first and second singleton deliveries we found that
women with a caesarean section at their first delivery were
at increased risk for retained placenta at their next delivery,
compared with women with a first vaginal delivery.
Women with previous caesarean delivery had an adjusted
OR of retained placenta with heavy bleeding (more than
1000 ml) of 1.61 (95% CI 1.441.79), but they had no
association with retained placenta with normal bleeding
(1000 ml or less). Retained placenta is associated with
increased morbidity and mortality for the mother.5,6 Our
findings highlight the importance to restrict caesarean sections to women in need of abdominal deliveries in order to
optimise delivery care.

Strengths and limitations


To our knowledge, our study is the first to separate
retained placenta with heavy bleeding from retained
placenta with normal bleeding. This distinction is important because of the increase in maternal morbidity and
mortality associated with severe postpartum haemorrhage.20
One limitation is the difficulty in estimating blood loss
during delivery, however, but this possible source of misclassification should be non-differential. Another major
strength of the study is the large population-based design
where data on exposure and confounding factors were collected prospectively, which limits the risk of recall bias. The
standardised and free antenatal and delivery care in Sweden
minimises the possibilities of residual confounding.
Another strength was the determination of a number of
possible confounding factors that could affect the association under study.814 We have also identified other risk factors for retained placenta, such as in vitro fertilisation and
interpregnancy interval, which were not accounted for in
previous studies.
One limitation is that data on prior terminations of
pregnancy were unavailable, as some studies report an
increased incidence of retained placenta in women with a
previous history of surgically induced abortions.21 However, in Sweden today 79% of induced terminations are
performed before gestational week 9, and 89% of these are
medically induced.22 As no association between retained
placenta and medically-induced terminations has been
shown,23 this limitation will probably have a marginal
effect on the studied association. Another limitation is that
there is no validation of the diagnosis of retained placenta
in the Swedish birth register; however, the incidence of
retained placenta found here is in agreement with the
Swedish study by Endler et al.,14 where the diagnosis was
set after a review of medical records.

228

Interpretation
The association between retained placenta and previous
delivery by caesarean section has been investigated in
previous studies.1014 Two Scandinavian casecontrol studies found no increased risk of retained placenta after a
caesarean section.11,14 These studies included both nulliparous and parous women, and none of the studies had previous caesarean sections as their main exposure. As these
reports included just 165 and 400 cases, the statistical power
was limited.11,14 A case-control study by Titiz et al.10 with
114 cases showed the same result. On the other hand, two
reports from Saudi Arabia and from New South Wales,
Australia, presented results well in line with ours.12,13 The
latter found an adjusted odds ratio of 1.34 for manual
removal of the placenta after a previous caesarean section.13
The pathophysiology underlying retained placenta can
either be a trapped placenta, where the placenta has been
detached from the uterine wall but trapped behind a closed
cervix, or a placenta adherent to the uterine wall.24 The fact
that we recorded an increased risk for retained placenta,
especially for cases with heavy bleeding, suggests that there
is an enhanced risk for placental adherence after a previous
caesarean section. The most severe form of adherence is
placenta accreta,24 which has a well-known association with
previous caesarean section.25
The mechanism behind the increased risk of retained
placenta by a previous caesarean section is unknown. It
was recently suggested that a uterine scar following caesarean section creates localised hypoxia, with subsequent
defective decidualisation and abnormal trophoblastic invasion.26 It is likely that this mechanism is similar for
retained placenta. Another theory is a contractile failure in
the retroplacental area as a result of the uterine scar.27
Using ultrasound, Herman et al. found that the myometrium on the placental site was thickened, from <1 to >2 cm,
in normal labour, but stayed thin in cases with retained
placenta.27 It is possible that a change in myometrial thickness is less likely to occur in the area of a uterine scar.
These theories are based on a direct effect of the uterine
scar on placental detachment. Thus, it would be interesting
to study placental location in the uterus and its impact on
the association between previous caesarean section and
retained placenta.

Conclusion
The finding of this study indicates that a previous caesarean section increases the risk of retained placenta with
heavy bleeding. Although we cannot exclude that this
increased risk may result from unmeasured confounding
factors, rather than the procedure itself, we suggest that
this information should be accounted for when an individual risk assessment is performed for a pregnant woman.

2013 Royal College of Obstetricians and Gynaecologists

Retained placenta and previous caesarean section

Awareness of complications in women previously delivered


by caesarean sections is key for influencing the increasing
number of caesarean sections worldwide. Our findings
enhance the need for more studies on the long-term effects
on reproductive health caused by caesarean sections.

Disclosure of interests
All authors report no conflict of interests.

Contribution to authorship
A-KW had the original idea for the study. SC contributed
with database management and expertise in epidemiology.
A-KW, JB, OA, KE, and AM-L contributed to the design of
the study. A-KW and JB performed the analyses and wrote
the first draft of the manuscript. SC, OA, KE, and AM-L
made substantial contributions to the interpretation of the
results and to manuscript revision.

Details of ethics approval


The research ethics committee at the Karolinska Institutet,
Stockholm, approved the study (ref. no. 2005/4863; 28
September 2005).

Funding
The research was funded by, Uppsala University and the
county council of Uppsala Sweden.

Supporting Information
Additional Supporting Information may be found in the
online version of this article:
Table S1. Adjusted risks of retained placenta according
to maternal, delivery, and infant characteristics at second
birth. &

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