Systematic Review and Meta-Analysis: PPH Incidence in Placenta Previa

This research article presents a systematic review and meta-analysis investigating the incidence of postpartum hemorrhage (PPH) in pregnant women diagnosed with placenta previa. The study, conducted according to MOOSE guidelines, analyzed data from 11 observational studies, encompassing 5146 unique pregnant women. The overall pooled incidence of PPH was found to be 22.3%. Subgroup analyses revealed variations in prevalence based on the type of placenta previa and geographical region. The research highlights the importance of understanding PPH incidence for prevention, treatment, and public health strategies. The study utilized four databases for literature searches and adhered to the PRISMA standard. Methodological quality was assessed using the STROBE guideline. Statistical analyses included both individual and pooled incidence calculations, with heterogeneity addressed through random effects meta-analysis. Sensitivity analysis and publication bias tests were also performed to ensure the reliability of the findings. The results of this systematic review are crucial in preventing, treating, and identifying PPH among pregnant women with placenta previa, and contribute to the planning and implementation of relevant public health strategies.

RESEARCH ARTICLE
The Incidence of Postpartum Hemorrhage in
Pregnant Women with Placenta Previa:
A Systematic Review and Meta-Analysis
Dazhi Fan1,2☯, Qing Xia2☯, Li Liu2,3, Shuzhen Wu1, Guo Tian3, Wen Wang1, Song Wu4,
Xiaoling Guo1‡* , Zhengping Liu1‡*
1 Department of Obstetrics, Southern Medical University Affiliated Maternal & Child Health Hospital of
Foshan, Foshan, Guangdong, China, 2 Department of Epidemiology and Biostatistics, School of Public
Health, Anhui Medical University, Hefei, Anhui, China, 3 Department of Library, the First Affiliated Hospital,
College of Medicine, Zhejiang University, Hangzhou, Zhejiang, China, 4 School of Integrated Traditional and
Western Medicine, Anhui University of Chinese Medicine, Hefei, Anhui, China
☯These authors contributed equally to this work.
‡ These authors also contributed equally to this work.
* [e-mail] (ZL); [e-mail] (XG)
Abstract
Background
The global burden of postpartum hemorrhage (PPH) in women with placenta previa is a
major public health concern. Although there are different reports on the incidence of PPH in
different countries, to date, no research has reviewed them.
Objective
The aim of this study was to calculate the average point incidence of PPH in women with pla-
centa previa.
Methods
A systematic review and meta-analysis of observational studies estimating PPH in women
with placenta previa was conducted through literature searches in four databases in Jul
2016. This study was totally conducted according to the MOOSE guidelines and in accor-
dance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses
standard.
Results
From 1148 obtained studies, 11 included in the meta-analysis, which involved 5146 unique
pregnant women with placenta previa. The overall pooled incidence of PPH was 22.3%
(95% CI 15.8–28.7%). In the subgroup, the prevalence was 27.4% in placenta previas, and
was 14.5% in low-lying placenta previa; the highest prevalence was estimated in Northern
America (26.3%, 95%CI 11.0–41.6%), followed by the Asia (20.7%, 95%CI 12.8–28.6%),
Australia (19.2%, 95% CI 17.2–21.1%) and Europe (17.8%, 95% CI, 11.5%-24.0%).
PLOS ONE | DOI:10.1371/journal.pone.0170194 January 20, 2017 1 / 15
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OPEN ACCESS
Citation: Fan D, Xia Q, Liu L, Wu S, Tian G, Wang
W, et al. (2017) The Incidence of Postpartum
Hemorrhage in Pregnant Women with Placenta
Previa: A Systematic Review and Meta-Analysis.
PLoS ONE 12(1): e0170194. doi:10.1371/journal.
pone.0170194
Editor: Cassandra Nichole Spracklen, University of
North Carolina at Chapel Hill, UNITED STATES
Received: August 31, 2016
Accepted: January 2, 2017
Published: January 20, 2017
Copyright: © 2017 Fan et al. This is an open access
article distributed under the terms of the Creative
Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in
any medium, provided the original author and
source are credited.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
files.
Funding: The author(s) received no specific
funding for this work.
Competing Interests: The authors have declared
that no competing interests exist.

Conclusions
The summary estimate of the incidence of PPH among women with placenta previa was
considerable in this systematic review. The results will be crucial in prevention, treatment,
and identification of PPH among pregnant women with placenta previa and will be contrib-
uted to the planning and implantation of relevant public health strategies.
Introduction
Placenta previa (PP) is characterized by the abnormal placenta overlying the endoc
and it is known as one of the most feared adverse maternal and fetal-neonatal com
obstetrics [1, 2]. All placentas overlying the os (to any degree) are termed previas
near to but not overlying the os are termed low-lying [3]. There appears to be an a
between endometrial damage and uterine scarring and subsequent placenta previ
while, the condition is frequently complicated by invasion of placental villi beyond
basalis causing placenta accreta or increta [5]. Placenta increta can unexpectedly
strophic blood loss, multiple complications, and even death [6]. Thus, women with
previa have often increased the risk of postpartum hemorrhage (PPH).
Postpartum hemorrhage (PPH) is a leading cause of global maternal morbidity a
ity [7]. Maternal deaths due to PPH have increased in many countries [8, 9, 10]. It
ing for about 30% of all pregnancy-related deaths in Asia and Africa [11, 12]. This
mortality rate has been attributed to a number of factors, including increasing age
at birth, the increasing multiple pregnancy rate as a consequence of artificial repro
techniques and the rising caesarean section rate [13, 14, 15]. The basic managem
consists of initial medical care and the use of uterotonic drugs and/or an intrauteri
[16]. When these initial therapies fail, second-line therapies, including intervention
ical techniques, uterine compression sutures, pelvic vessel ligation or new medical
such as recombinant activated factor VII (rFVIIa), may be used before hysterectom
ered to control bleeding avoid maternal death [17, 18]. Although little was known u
recently about the effectiveness of these therapies in practice, it was [19] demons
uterine compression sutures and interventional radiological techniques experience
success rates than rFVIIa and pelvic vessel ligation using a prospective cohort of w
PPH identified through UK Obstetric Surveillance System (UKOSS).
A reliable estimate of the incidence of PPH is important for informing efforts to p
treat, and identify causes of PPH among pregnant women with placenta previa and
be contributing to the planning and implantation of relevant public health strategie
fore, this study is designed to systematically review the relevant present studies w
reported the incidence of PPH in pregnant women with placenta previa and has a p
analysis of the prevalence in the overall population and subgroups of the participa
attempt is also made to identify risk factors for the incidence of PPH by applying m
regression analyses to the available data.
Materials and Methods
This systematic review was conducted according to the MOOSE guidelines [20] and
dance with the Preferred Reporting Items for Systematic Reviews and Meta-Analys
Incidence of PPH in PP
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(PRISMA) standard [21]. Supporting information showed the protocol and checklist
tocol and S1 Checklist).
Search strategy and selection criteria
Two independent authors (DF, LL) searched PubMed, Elsevier Science Direct, Coch
Library and the Chinese National Knowledge Infrastructure database (CNKI) from d
inception to 31 Jul 2016. Key words used were “placenta previa” OR “Low-lying pla
“PP” AND “hemorrhage” OR “haemorrhage” OR “vaginal bleeding” AND “postpartu
the title, abstract or index term fields. An example for the complete search strateg
PubMed search was presented in S1 Search Strategy. There were no language rest
time restrictions. Relevant eligible literatures were also scanned through cross-refe
identification in the reference lists within both original and review articles.
We included observational studies (cross-sectional, retrospective and prospectiv
in participants that fulfilled the following criteria: (a) placenta previa was defined a
that by ultrasound was partially or completely covering the internal os of the cervi
(b) PPH diagnosis according to blood loss of more than 500 ml for vaginal deliverie
than 1000 ml for cesarean delivery by the American College of Obstetricians and G
gists (ACOG) [22]. For estimation of the incidence of PPH, we excluded studies with
standardized diagnoses, (b) non-standardized definitions of PPH, (c) insufficient da
extraction of PPH rates. The studies were also excluded based on the following crit
reports, letters, review articles or editorials; or the full data was not accessible eve
from the primary/corresponding authors. In the case of multiple publications from
study, only the most comprehensive paper or article with the largest sample size o
follow-up was considered.
Data extraction
After initial evaluation, two reviewers (DF and SW) independently and carefully eva
articles and performed the data extraction according to the selection criteria. We e
following variables: first author, year of publication, survey years, study country, a
(mean ± standard deviation or median, range), the number of cases of PPH and th
placenta previa sample size. When discrepancies existed, discussion was performe
tation with another reviewer (ZL) until a consensus was reached.
Methodological quality assessment
The methodological quality of each study was independently assessed by two revie
and QX) via the Reporting of Observational Studies in Epidemiology (STROBE) guid
which was used in previous meta-analysis [24], including our team [2]. The STROB
line, which was a checklist of 22 items, included 5 core components (sample popul
ple size, participation rate, outcome assessment, and analytical methods to contro
Each core component has three options: low risk (score = 2), moderate risk (score
high risk (score = 0) (S1 Table). The total score which ranged from 0 to 10, represe
summary assessment of bias risk for each study. When there was a disagreement,
by consensus of the whole team.
Statistical analyses
Individual and pooled incidence as well as 95% confidence interval (95%CI) were c
for each of all the included studies using the STATA 12.0 (Stata-Corp, College Stati
Incidence of PPH in PP
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USA). Before performing an inverse-variance weighted, the incidence was transform
the Freeman-Tukey double arcsine method [25]. Due to anticipated heterogeneity,
dom effects meta-analysis was employed. The inverse variance methods and DerS
Laird random-effects model meta-analysis was used to determine the weight of ea
[26]. Statistical heterogeneity was evaluated by the chi-square test on Q statistic,
quantified by the I-square values, assuming that I-square values 25, 50 and 75% w
nally assigned as low, moderate, and high estimates, respectively [27]. To investig
tial sources of heterogeneity, subgroup analyses and meta-regression were perform
find any possible sources using the following grouping variables: type of placenta p
geographical region, maternal age, gestational week, data collection period, perce
potential characteristics (prior cesarean sections, multiparous, and anterior positio
centa) and study quality. Furthermore, in the entire dataset, we conducted subgro
ses (including χ2 tests, odds ratios) to investigate different types of placenta previa an
geographical regions. Sensitivity analysis was performed to assess whether one or
studies influenced the overall results. Potential publication bias was tested using th
plot and the method of Egger’s regression and Begg’s test. P 0.05 indicated the pr
statistically significant.
Results
Characteristic results
Our search yielded 1148 publications of which 11 studies including 14 unique PPH
lence rates, met inclusion criteria (Fig 1). Five took place in North America [28–32]
Asia [6, 33, 34], two in Europe [35, 36], and one in Australia [37] (Table 1). The art
published between 2000 and 2016, and the final sample comprised 5146 unique p
women with placenta previa. Sample sizes ranged from 95 to 1612 participants wi
sample size of 488. Mean age was 31.89 years (range = 29.78–34.20 years), and m
tion age was 37.77 weeks (35.40–39.40). Five studies [28, 29, 34–36] reported ant
centa frequencies and 36.05% of women (n = 860) were anterior placenta. 29.67%
were prior cesarean delivery (n = 954), 67.73% of women were multiparae (n = 33
6.85% of women were accompanied with placenta accrate. Six studies [28, 29, 31,
(n = 1329) including women were diagnosed with low-lying placenta previa. The p
of PPH ranged from 3.6% [31] to 58.7% [30]. When evaluated by STROBE quality a
criteria, two studies [33, 37] received 9 points, five [29–31, 34, 35] received 8 poin
[6, 28, 32, 36] received 7 points (S2 Table). The quality scores showed that studies
acceptable quality.
Meta-analysis results
The overall pooled incidence was 22.3% (95% CI 15.8–28.7%). The I2 statistic (97.6%,
P < 0.001) indicated substantial heterogeneity (Fig 2). The graphical funnel plots a
to be symmetrical (Fig 3), and the Begg (z = 0.18, P = 0.855) and Egger test (t = -
P = 0.263) indicated there was no strong evidence for publication bias. To confirm
stability and liability of the meta-analysis, sensitivity analysis was performed by re
the calculation pooled PPH incidence when any single study was deleted. Fig 4 sho
the corresponding pooled incidence ranged from 19.7% (13.7–25.8%) to 25.4% (19
31.6%) and was not substantially altered. The statistically similar resulted indicate
each single study didn’t influence the stability of overall PPH incidence estimate in
meta-analysis.
Incidence of PPH in PP
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Subgroup results
The PPH incidence was further analyzed by subgroup according to different types o
previa and world regions. The PPH incidence was 27.4% (95%CI 20.2–34.5%, n = 32 =
95.8%) in placenta previas, and was 14.5% (95%CI 7.0–22.1%, n = 1329, I2 = 93.6%) in low-
lying placenta previa (Table 2 and Fig 5). The PPH incidence was lower in low-lying
previa (OR = 0.36, 95%CI 0.30–0.44, P = 0.001). Regarding the potential variation
world regions, the highest PPH incidence was estimated in Northern America (26.3
11.0–41.6%, I2 = 98.9%), followed by the Asia (20.7%, 95%CI 12.8–28.6%, I2 = 88.7%), Austra-
lia (19.2%, 95% CI 17.2–21.1%, based on a single study) and Europe (17.8%, 95%
24.0%, I2 = 35.6) (Table 2 and Fig 6). However, it was found no difference in PPH inci
among the world regions (P = 0.227).
Fig 1. PRISMA flowchart showing the study selection process.
doi:10.1371/journal.pone.0170194.g001
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Meta-regression
A high level of heterogeneity between studies and subgroups was observed. Meta-
was performed to explore potential sources of heterogeneity. Maternal age, gestat
year of data collection, quality score, and percentage of anterior placenta (%), prio
section (%), multiparous (%), placenta accreta (%), and smoking (%), which may b
sources of heterogeneity, were tested by meta-regression method. Through the re
model, except for prior cesarean section (P = 0.044), none of aforementioned varia
nificantly associated with the detected heterogeneity (Table 3). We, therefore, furt
the correlation between the percentage of prior cesarean section and the PPH incid
found that there was a positive correlation between the percentage of prior cesare
and the PPH incidence (r = 0.879, P = 0.049).
Table 1. Characteristic of included studies in meta-analysis.
Source Cases Total Age* (years) GA* (weeks) AP PCS PA MP Somking Survey
Period
P (95%
CI)
country QS
Zhao L, 2016
[33]
54 312 29.85±2.62 32.62±3.76 — 30 17 211 — 2012–
2015
0.17
[0.13–
0.22]
China 9
Wortman AC,
2016 [28]
42 98 30.75±6.10 38.07±2.30 18 21 — 80 3 2002–
2012
0.43
[0.33–
0.53]
USA 7
Ji XL, 2015
[34]
43 112 32.00±5.43 — 38 34 27 80 — 2010–
2014
0.38
[0.29–
0.47]
China 8
Osmundson
SS, 2013 [29]
36 353 33.10±5.20 39.20±1.80 143 — — 186 — 2009–
2010
0.10
[0.07–
0.13]
USA 8
Ge J, 2012 [6] 213 1121 33.40±7.80 — — — — — — 2005–
2010
0.19
[0.17–
0.21]
China 7
Vergani P,
2009 [35]
20 95 34.18±5.60 36.78±4.30 46 — — 36 — 2003–
2008
0.21
[0.13–
0.29]
Italy 8
Zlatnik MG,
2007 [30]
135 230 162 (70.4%) <35
years; 68 (29.6%)
35 years
35.40±2.50 — 180 — 135 — 1980–
2001
0.59
[0.52–
0.65]
USA 8
Tuzovic L,
2006 [36]
32 202 75 (37.1%) <30
years; 127 (62.9%)
>30 years
119 (58.9%) >37 weeks;
47 (23.3%): 34–37 weeks;
17 (8.4%): 32–34 weeks;
11 (5.5%): 30–32 weeks; 8
(4.0%) <30 weeks
65 20 14 170 40 1992–
2001
0.16
[0.11–
0.21]
Croatia 7
Olive EC,
2005 [37]
309 1612 14 (0.9%) <20
years; 1030
(63.9%):20–34
years; 568 (35.2%)
35 years
937 (58.1%) 37 weeks;
561 (34.8%):32–36 weeks;
93 (5.8%):28–31 weeks;
21 (1.3%):26–27 weeks
— — — 1118 — 1998–
2002
0.19
[0.17–
0.21]
Australia 9
Ogueh O,
2003 [31]
25 703 31.30±4.80 39.40±1.80 — 82 — — 76 1997–
1999
0.04
[0.02–
0.05]
Canada 8
Crane JM,
2000 [32]
56 308 30 — — 69 6 234 106 1988–
1995
0.18
[0.14–
0.22]
Canada 7
AP: placenta on anterior wall; GA: gestational age; MP: multiperous; PA: placenta accrate; PCS: previous cesarean section; QS: quality score;
* Values indicate the mean (range), or mean±standard deviation;
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Discussion
The aim of this systematic review and meta-analysis is to study the present status
dence of postpartum hemorrhage (PPH) in pregnant women with placenta previa (
explore the determinants of PPH incidence. To our knowledge, this systematic revi
first meta-analysis and provides a comprehensive overview of the current literatur
the data of 11 articles including 14 unique studies, PPH incidence rate (22.3%) rem
approximately 4-fold higher than among all women, in pregnant women with place
With reference to types of placenta previa, lower PPH incidence rate was demonstr
low-lying placenta pregnant women (14.5%). When evaluated by study region, the
was high in North America (26.3%), intermediate in Asia (20.7%) and Australia (19
low in Europe (17.8%). In addition, it was also found that prior cesarean section as
with increased risk for PPH.
In 2008, a systematic review was published on the incidence of PPH with the obj
evaluating its magnitude both globally and in different regions [8]. Based on the re
incidence was believed to be around 6% in observational studies. However, there w
variation across the different regions of the world, ranging from 2.55% in Asia to 1
Fig 2. Forest plot of pooled estimated incidence of PPH with 95% CI.
doi:10.1371/journal.pone.0170194.g002
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Africa. It was believed that risk factors for PPH included uterine atony, genital tract
coagulation abnormalities, past history of PPH, multiple gestations and placental a
ties, such as placenta previa or placenta accreta [13, 38, 39].
Several studies have estimated the incidence of PPH among pregnant women w
previa in different countries [30, 32, 33, 35]. However, there was a wide variation i
of the conducted studies. The incidence of PPH was reported to be approximately 1
Canada population-based retrospective cohort study among 308 cases of placenta
21% in a Italy retrospective singleton pregnancies cohort between January 2003 an
2008 [35] and 59% in a USA retrospective singleton births cohort that occurred be
and 2001 among the 230 placenta previa women [30].
Some studies have also focused on the association between placenta type and t
PPH. However, the results for this have been inconclusive. Ogueh et al [31] reporte
dence of PPH was only 3.56%, lower than among all women (6%), in a low-lying pla
women. Zlatnik et al [30] reported placenta previa was associated with PPH and th
was even 10-fold higher (58.69%) for placenta previa than among all women. Risk
wide variation include data collection period, sample size, placenta type, geograph
and other potential characteristics, such as prior cesarean sections, multiparous an
week.
Fig 3. Funnel plot of the 11 studies included in the meta-analysis.
doi:10.1371/journal.pone.0170194.g003
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Abnormal placentation has been observed to be associated with previous caesar
ies or other uterine surgeries, such as myomectomy or curettage, advanced mater
multiparity [4]. Previous studies have reported that these factors were associated
increased risk of PPH [13, 15, 38, 39]. In this study, our finding support existing ev
showing that prior cesarean section increases the risk of PPH by a system review a
analysis. However, similarly result was not found in other factors. The discrepancy
Fig 4. Sensitivity analysis for individual studies on the summary effect.
doi:10.1371/journal.pone.0170194.g004
Table 2. Results of subgroup analysis for the incidence of postpartum hemorrhage.
Variable Number of surveys Total Cases P (95% CI) I2 (%)
Placenta types
PP 8 3817 842 0.27[0.20–0.35] 95.8
LPP 6 1329 123 0.15[0.07–0.22] 93.6
Regions
Asia 5 1545 310 0.21[0.13–0.29] 88.7
Australia 1 1612 309 0.19[0.17–0.21] —
Europe 3 297 52 0.18[0.12–0.24] 35.6
Northern America 5 1692 294 0.26[0.11–0.42] 98.9
PP: placenta previa; LPP: low-lying placenta previa;
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reflect a lack of statistical power in this system review owing to the small number
other above factors.
The systematic review and meta-analysis included 11 articles including 14 uniqu
with a large sample size, and it showed no potential risk of publication bias. The ov
of the studies included was all acceptable, therefore, the result of sensitivity analy
substantially altered. Nevertheless, there are limitations due to the heterogeneity
considered when interpreting the findings of this study.
The primary limitation of this meta-analysis was that significant heterogeneity b
studies was observed in the study, which was not surprising as heterogeneity often
such meta-analysis of overall prevalence [40–42]. Although subgroup and meta-re
analyses did indicate that percentage of prior cesarean section to explain the obse
geneity, the remainder among the studies could be unexplained by the variable ex
ther analyses could not be performed, because of the limited information on these
Fig 5. Funnel plot by subgroup analysis of placenta types. PP: placenta previas; LPP: low-lying placenta previa.
doi:10.1371/journal.pone.0170194.g005
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addition, the results relied on aggregated published data. Further large-scale, mult
spective study using a single validated measured of PPH in a random subset of par
would provide a more accurate estimate of the incidence of PPH in women with pla
previa.
In conclusion, the summary estimate of the incidence of PPH among women with
previa was considerable in this systematic review. The results will be important for
efforts to prevent, treat, and identify causes of PPH among pregnant women with p
via and would be contribute to the planning and implantation of relevant public he
strategies.
Fig 6. Funnel plot by subgroup analysis of world regions.
doi:10.1371/journal.pone.0170194.g006
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Supporting Information
S1 Checklist. PRISMA Checklist.
(DOC)
S1 Protocol. Protocol.
(DOC)
S1 Search Strategy. The PubMed search strategy.
(DOCX)
S1 Table. The items of the chosen system for quality assessment of the in
(DOC)
S2 Table. The score assignment to included studies.
(DOC)
Acknowledgments
We appreciate the efforts of all the researchers whose articles were included in thi
Author Contributions
Conceptualization: ZL XG.
Data curation: DF QX.
Formal analysis: DF Song W. QX LL.
Funding acquisition: ZL XG.
Investigation: LL Shu-Zhen W. GT WW.
Methodology: DF Song W.
Project administration: DF ZL.
Resources: QX Shu-Zhen W.
Software: DF QX LL.
Supervision: ZL XG.
Table 3. Results of meta-regression for the incidence of postpartum hemorrhage.
Covariate coefficient 95% CI t-value P-value
Age(year) 0.0060 -0.0415–0.0534 0.29 0.779
GA(week) -0.0120 -0.0890–0.0570 -0.42 0.686
Survey year -0.0040 -0.0163–0.0083 -0.71 0.490
QS -0.0319 -0.1631–0.0994 -0.53 0.606
AP -0.0103 -1.1385–1.1180 -0.04 0.972
PCS 0.6088 0.0285–1.1891 3.34 0.044
MP -0.0768 -1.6342–1.4805 -0.13 0.904
PA 1.1018 -0.8807–3.0843 2.39 0.139
Smoking -0.7846 -7.4064–5.8372 -1.51 0.373
AP: placenta on anterior wall; GA: gestational age; MP: multiperous; PA: placenta accrate; PCS: previous cesarean section; QS: quality score;
doi:10.1371/journal.pone.0170194.t003
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