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J Matern Fetal Neonatal Med, Early Online: 1–6

! 2014 Informa UK Ltd. DOI: 10.3109/14767058.2014.937698

ORIGINAL ARTICLE

Risk factors for early postpartum hemorrhage (PPH) in the first vaginal
delivery, and obstetrical outcomes in subsequent pregnancy
Naama Buzaglo1, Avi Harlev1, Ruslan Sergienko2, and Eyal Sheiner1
J Matern Fetal Neonatal Med Downloaded from informahealthcare.com by University of Washington on 10/26/14

1
Department of Obstetrics and Gynecology, Faculty of Health Sciences and 2Department of Epidemiology and Health Services Evaluation, Faculty of
Health Sciences, Soroka University Medical Center, Ben-Gurion University of the Negev, Israel

Abstract Keywords
Objective: To investigate risk factors for postpartum hemorrhage (PPH) in vaginal deliveries and Post-partum hemorrhage, post-term
the influence of previous PPH on the subsequent pregnancy. pregnancy, previous PPH, risk factors
Study design: A retrospective cohort study including first singleton deliveries between the years
1988 and 2012 was performed comparing deliveries with and without PPH. In addition, History
perinatal outcomes of the subsequent pregnancy were evaluated. Multivariable analysis was
performed to control for confounders. Received 1 April 2014
Results: PPH complicated 0.8% of all first vaginal deliveries. Significant risk factors for PPH in Revised 1 June 2014
vaginal delivery, using a multiple logistic regression model, were: post-term pregnancy, fertility Accepted 19 June 2014
treatments, hypertensive disorders, labor dystocia during the 2nd, and perineal tears grade 2 Published online 5 August 2014
and 3, respectively. Previous PPH was found to be an independent risk factor for PPH in the
For personal use only.

subsequent pregnancy. Moreover, previous PPH was found to be a significant risk factor for
cesarean section (CS) deliver, to complicate delivery with revision of uterus cavity, anemia, and
to require blood transfusion.
Conclusion: Previous PPH poses a risk for recurrent PPH in subsequent delivery and an increased
risk for CS. As PPH remains one of the major causes of maternal morbidity, this study
strengthens the need for a comprehensive evaluation of prior PPH as a major risk factor for PPH
recurrence.

Introduction responsible for 70–90% of all PPH cases [2,5,6]. Postpartum

hemostasis is based on powerful and prolonged hormonally-
Postpartum hemorrhage (PPH) is a life-threatening event
mediated contractions that decrease the blood flow to the
involving severe bleeding during and after the third stage of
placental bed [7,8].
labor. PPH is one of the most common obstetrical compli-
The major risk factors for PPH include over-distended
cations, affecting up to 18% of deliveries. It accounts for 35–
uterus (i.e. macrosomia, multiple gestations, hydramnios,
55% of peripartum maternal deaths worldwide [1].
etc.), prolonged or precipitous labor and chorioamnionitis [2].
Traditionally, early PPH is defined as blood loss exceeding
Nevertheless, atonic PPH occurs in more women without
500 ml within 24 h after vaginal delivery, or blood loss
known risk factors than those with identifiable risk factors
exceeding 1000 ml following cesarean section (CS) [2]. PPH
[9,10]. Additional causes of PPH include genital tract trauma
may cause short- and long-term maternal morbidity, including
(cervix, vagina or perineum); retained placental tissue; uterus
acute renal failure, hypovolemic shock, consumptive coagulo-
inversion, or ruptured uterus [2,6,11]. The different causes of
pathy, disseminated intravascular coagulation (DIC), blood
PPH can be explained by the 4T’s theory: Tone (uterine
transfusion related complications, or hysterectomy leading to
atony), Trauma (including genital tract trauma, uterine
loss of childbearing potential [3,4]. Approximately 12% of
rupture and uterine inversion, causing 20% of all cases),
women who survive a PPH event will suffer from anemia [4].
Tissue (retained placental products or blood clots, accounting
The most common cause of PPH is uterine atony, i.e.
for 6–10% of all cases) and Thrombin (coagulation abnorm-
failure of the uterus to contract adequately after birth,
alities, accounting for 1% of all PPH cases) [11,12].
Predicting PPH by risk factors is difficult because two-
thirds of women who have PPH actually manifest no risk
factors [13]. In addition to over-distended uterus, predispos-
ition to uterine muscle exhaustion include prolonged labor or
Address for correspondence: Avi Harlev, MD, Department of Obstetrics
and Gynecology, Soroka University Medical Center, POB 151, Beer rapid labor; functional/anatomical distortion of the uterus as
Sheva 84101, Israel. E-mail: harlev@bgu.ac.il in fibroid uterus, or placenta previa and chorioamnionitis.
 2 N. Buzaglo et al.
Induction of labor and prolonged treatment with oxytocin
were found to be independent risk factors for PPH [14].
Stones et al. analyzed factors associated with major obstetric
hemorrhage in a population of 37 497 women [15]. Factors
associated with significant risk for PPH were placental
abruption (RR 12.6; 99% CI, 7.61–20.9), placenta previa
(RR 13.1; 99% CI, 7.47–23.0), multiple pregnancy (RR 4.46;
99% CI, 3.01–6.61) and obesity (RR 1.64; 99% CI, 1.24–
2.17). Although multiparity was once thought to be a risk
factor for PPH, no significant risk was demonstrated in
this study.
Different preventive interventions have been studied as part
of the active management approach, including the administra-
tion of uterotonic agents after delivery, early cord clamping
and controlled cord traction of the umbilical cord [16–18]. The
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American College of Obstetricians and Gynecologists
(ACOG), the World Health Organization (WHO) and the
International Federation of Gynecologistsand Obstetricians
(FIGO) have published recommendations and guidelines
for active management of the third stage of labor (AMTSL)
[9,19–23].
Studies on long-term complications of PPH are limited and
include mainly the risk of recurrent PPH and infertility due to
the life-saving techniques used to manage the event [24–27].
It seems that PPH in a previous pregnancy is a major risk
factor for recurrent PPH in a subsequent pregnancy (RR, 3.3;
95% CI, 3.1–3.5), although scarce data exist [27]. Fullerton
For personal use only.
et al. found a significant reduction in the proportion of women
conceiving after a CS in their first pregnancy complicated by
PPH [28]. Despite marked improvements in prevention and
management, early PPH remains a significant contributor to
maternal morbidity and mortality both in developing
countries and in high resources areas [20].
The lack of prenatal care (LOPC) characterizes traditional
religious societies and has already been identified to be
associated with adverse obstetric outcomes and specifically as
an independent risk factor for perinatal mortality [29]. Since a
minority of religious Bedouin Arabs lives in the southern of
Israel, where this study was conducted, the association
between LOPC and PPH was evaluated.
This study aims to investigate risk factors for PPH. In
addition, it aims to study the influence of previous PPH on the
subsequent pregnancy. Identifying risk factors may improve
prevention and management practices of one of the major
causes of maternal mortality.
Materials and methods
A population-based study comparing all first singleton
deliveries that took place at the Soroka University Medical
Center between the years 1988 and 2012 was conducted. The
perinatal outcomes of the subsequent pregnancy were
evaluated as well. The data were retrieved from the
computerized database of the Department of Obstetrics and
Gynecology. The database includes extensive information on
the antepartum, intra-partum, and postpartum course at the
hospital, assembled from computer-adapted medical record
forms and the patient’s perinatal and hospitalization records.
Early PPH was defined traditionally as blood loss exceed-
ing 500 ml within 24 h after vaginal delivery, according to the
J Matern Fetal Neonatal Med, Early Online: 1–6
charts. The following maternal and demographic characteris-
tics were evaluated: maternal age, ethnicity, gravidity, gesta-
tional age, lack of prenatal care, smoking, fertility treatments,
hypertensive disorders, diabetes mellitus (gestational and pre-
gestational). Gestational and delivery complications that were
investigated included induction of labor, premature rupture of
membranes (PROM), placental abruption, adherent placenta,
labor dystocia (failure to progress) during the 1st and 2nd
stages, shoulder dystocia, instrumental delivery and cervix
and birth canal lacerations.
The following neonatal characteristics were evaluated:
birth weight, perinatal mortality, Apgar score less than 7 at 1
and 5 min and non-reassuring fetal heart rate monitoring. The
following birth outcomes were recorded: episiotomy, retained
placenta, manualysis, blood transfusions and hemoglobin
level at discharge from the hospital.
Statistical analysis was performed with the SPSS package
version 17 (SPSS, Chicago, IL). Univariate analysis was
carried out by X2 tests for categorical variables and t-test for
normally-distributed variables. Multivariate analysis was
conducted by logistic regression models, in order to find
independent risk factors for PPH while controlling for
confounders. p value 50.05 was considered statistically
significant.
Results
A total of 56 394 first vaginal deliveries occurred during the
study period. PPH complicated 0.79% of all 1st vaginal
deliveries were included in this study. Demographic and ethnic
characteristics did not differ between the groups (Table 1).
Pregnancy characteristics of women of the two study
groups are presented in Table 2. Women belonging to the PPH
group were more likely to conceive after fertility treatments
and had more post-term pregnancies. Women in the PPH
group showed a higher rate of hypertensive disorders, PROM
and labor induction. Labor complications and adverse peri-
natal outcome including non-progressive labor (NPL) stage 2,
perineal tears grade 2–3, and adherent placenta were found to
be significantly increased in the PPH group. This group also
underwent more vacuum deliveries. Furthermore, women
belonging to the PPH group were more likely to undergo
revision of uterus and cervix and manualysis of the placenta.
In addition, women in the PPH group were found to have a
significantly higher rate of anemia and required blood
transfusion during hospitalization. High rates of episiotomy
were found in both groups. While comparing neonatal
outcomes, macrosomia and non-reassuring fetal heart rate
monitoring were found to be statistically higher in the PPH
group (Table 3).
Using a multiple logistic regression model to control for
confounders, post-term pregnancy, fertility treatments, hyper-
tensive disorders, NPL stage 2 and perineal tears were found
to be independent risk factors for PPH in first vaginal delivery
(Table 4).
Maternal and pregnancy characteristics of second sub-
sequent deliveries after first vaginal delivery with PPH
were evaluated as well. Repeated PPH was more prevalent
in these women (Table 5). Women in this group were
more likely to have a CS delivery, to undergo revision of
 DOI: 10.3109/14767058.2014.937698 Risk factors for postpartum hemorrhage 3
Table 1. Maternal characteristics of first vaginal deliveries with and without PPH.

PPH No. of No PPH No. of

1st Deliveries ¼ 447 1st Deliveries ¼ 55 947 p value
Age, years ± SD 24.5 ± 4.5 24.1 ± 4.3 0.630
Gestational Age, weeks ± SD 39.3 ± 2.1 38.9 ± 2.4 0.002
Gestational Age in weeks
0–36 6.7% 8.9% 0.004
37–41 87.7% 87.9%
42+ 5.6% 3.1%
Ethnicity
Jewish 63.1% 60.3% 0.125
Bedouins 36.9% 39.7%
Gravidity
1 84.1% 83.9% 0.399
2–4 15.2% 15.8%
5+ 0.7% 0.3%
Lack of prenatal care 3.6 % 5.1% 0.088
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Self-reported smoking status 0.9% 0.9% 0.603

Table 2. Pregnancy and obstetric characteristics of first vaginal deliveries with and without PPH.

PPH No. of 1st No PPH No. of 1st

Deliveries ¼ 447 Deliveries ¼ 55 947 p value
Fertility treatments
OI 1.6% 1.1% 0.001
IVF 5.6% 2.7% 0.001
Hypertensive disorder 9.8% 6.6% 0.004
Diabetes mellitus (gestational and pregestational) 4.5% 3.7% 0.238
PROM 17% 13% 0.007
NPL STAGE 1 0.0% 0.1% 0.625
For personal use only.

NPL STAGE 2 7.4% 2.9% 50.001

Adherent placenta 1.8% 0.7% 0.013
Perineal tear grade 2 13.9% 6% 50.001
Perineal tear grade 3 1.8% 0.3% 50.001
Episiotomy 39.6% 49.2% 50.001
Cervical tear 8.7% 0.4% 50.001
Oxytocin treatment during delivery 43.2% 37.9% 0.012
Induction of Labor 51.5% 44.4% 0.002
Anemia (Hemoglobin level 510) 72.5% 29% 50.001
Blood transfusion 25.7% 1.1% 50.001
Placental abruption 0.2% 0.3% 0.675
Vacuum delivery 15.4% 9.1% 50.001
Shoulder dystocia 0.2% 0.1% 0.328

PROM – Premature rupture of membranes, NPL – Non-progressive labor.

Table 3. Neonatal outcomes of first vaginal deliveries with and without PPH.

PPH No. of 1st No PPH No. of 1st

Deliveries ¼ 447 Deliveries ¼ 55 947 p value
Perinatal Mortality 1.8% 1.5% 0.383
Low AP1 (57) 6.0% 4.8% 0.123
Low AP5 (57) 2.5% 1.9% 0.239
Birth weight
52500 5.4% 10.9% 50.001
2500–3999 88.4% 87.3%
4¼ 4000 6.3% 1.8%
Non-reassuring fetal heart rate monitor 8.1% 5% 0.003

AP1 – Apgar score at 1st second, AP5 – Apgar score at 5th second.

uterus and cervix, have higher rates of anemia, and were
more likely to require blood transfusion. Neonatal out-
comes of second subsequent deliveries after first vaginal
deliveries with PPH did not differ from the control group
(Table 6).
The effect of previous PPH on subsequent delivery was
adjusted to possible confounders in a multivariate analysis.
Previous PPH was found to be an independent factor for
PPH in the subsequent pregnancy (OR 8.49, CI 4.79–15.04,
p50.001).
 4 N. Buzaglo et al. J Matern Fetal Neonatal Med, Early Online: 1–6

Discussion singleton vaginal delivery complicated by PPH (weighted OR

8.49, CI 4.79–15.04, p50.001). Surprisingly, unlike the
The current study found a considerably higher risk for a
higher rates of PPH described in the literature, the relatively
recurrent PPH in subsequent vaginal delivery after previous
low rate of PPH found in our study, involving 0.79% of all
women in first vaginal deliveries, may be explained by the
Table 4. Risk factors for PPH in 1st vaginal delivery, by multiple logistic selected population of first singleton vaginal deliveries. This
regression model.
low rate of PPH can also be attributed to underestimation of
Characteristics OR 95% CI p value
blood loss during vaginal delivery.
Recent literature shows a strong association between
Post-term 42+ weeks 1.9 1.2–2.8 0.002 previous PPH and the need for fertility treatments in
Fertility treatments 1. 9 1.3–2.7 0.001
Hypertensive disorders 1.6 1.1–2.1 0.006 subsequent pregnancy as a consequence of embolization, B-
PROM 1.4 1.0–1.7 0.012 lynch and other life saving techniques used to manage the
NPL 2nd stage 2.6 1.8–3.7 50.001 PPH. Our study did not find any significant difference in the
Perineal tear grade 2 2.529 1.9–3.3 50.001
rate of fertility treatments after previous PPH. However,
Perineal tear grade 3 5.2 2.5–10.6 50.001
Labor induction 1.2 0.9–1.4 0.079 women were more likely to suffer from PPH following
J Matern Fetal Neonatal Med Downloaded from informahealthcare.com by University of Washington on 10/26/14

successful fertility treatments in their initial pregnancy.

PROM – Premature rapture of membranes, NPL – Non-progressive labor Induction of labor is a well-known risk factor for PPH [14],

Table 5. Maternal characteristics at subsequent deliveries (after first vaginal deliveries with PPH).

PPH in last pregnancy No PPH in last pregnancy

No. of patients ¼ 302 No. of patients ¼ 40 247 p value
Age, years ± SD 26.0 ± 4.3 26.1 ± 4.6 0.577
Gestational age, weeks ± SD 39.1 ± 1.8 38.9 ± 2.2 0.306
Gestational age in weeks
0–36 6.3% 8.2% 0.440
37–41 90.4% 89.1%
For personal use only.

42+ 3.3% 2.8%

Ethnicity
Jewish 57.3% 56.4% 0.407
Bedouins 42.7% 43.6%
Gravidity
2–4 98% 97.9% 0.567
5+ 2% 2.1% 0.567
Fertility treatments 3.6% 2.3% 0.092
Hypertensive disorders 2% 3.3% 0.127
PROM 9.9% 7.3% 0.051
NPL Stage 1 0.0% 0.5% 0.222
NPL Stage 2 1.3% 0.5% 0.088
Adherent placenta 1.3% 0.6% 0.102
CS 10.6% 6.2% 0.001
Manuallysis of the placenta 5.6% 1.8% 50.001
Oxytocin treatment during delivery 24.5% 21% 0.078
Induction of labor 29.5% 25.7% 0.074
PPH 4.3% 0.5% 50.001
Anemia (Hemoglobin level 510) 39.1% 27.8% 50.001
Blood transfusion 4% 1% 50.001

PROM – Premature rapture of membranes, NPL – Non-progressive labor.

Table 6. Obstetrical and neonatal outcomes in subsequent deliveries (after first vaginal deliveries with PPH).

PPH in last pregnancy No PPH in last pregnancy

No. of patients ¼ 302 No. of patients ¼ 40 247 p value
Perinatal mortality 0.7% 1.0% 0.388
Low AP1 (57) 3.0% 4.4% 0.149
Low AP5 (57) 1.7% 2.3% 0.304
Fetal weight, grams
52500 5.3% 8.1% 0.061
2500–3999 89.4% 88.3% 0.061
4000 5.3% 3.5% 0.061
Placental abruption 0.0% 0.5% 0.210
Non-reassuring fetal heart rate monitor 3.0% 2.8% 0.492
Vacuum delivery 1.3% 1.7% 0.424
Shoulder dystocia 0.3% 0.2% 0.429
 DOI: 10.3109/14767058.2014.937698
due to the use of uterogenic drugs and prolonged first stage of
labor. We found significantly higher rates of PPH in women
who underwent induction of labor. However, after using a
multiple logistic regression model controlling for confoun-
ders, induction of labor was not found to be an independent
risk factor for PPH.
Preeclampsia is a well-established risk factor for PPH
[14,24]. In our study, using a multiple logistic regression
analysis, hypertensive disorders were found to be an inde-
pendent risk factor for PPH. A possible mechanism for the
association between the hypertensive disorder and PPH may
be the pathological placentation [30,31], thought to be an
underlying cause for preeclampsia and a possible cause of
placental abruption or abnormal placental separation after
delivery.
J Matern Fetal Neonatal Med Downloaded from informahealthcare.com by University of Washington on 10/26/14
Other independent risk factors for PPH were post-term
pregnancies and prolonged 2nd stage. Post-term delivery as a
cause for PPH can be explained by the impaired placental
function which characterizes post-term pregnancy. The
second stage of labor is characterized by the presence of
frequent and prolonged contractions, which can contribute to
fetal distress and the need for instrumental delivery as a
consequence resulting in PPH. In addition, possible trauma to
the genital tract can accompany a prolonged second stage of
labor following the use of episiotomy or spontaneous tears.
High rates of episiotomy seen in both groups can be explained
by the protocol for routine use of this procedure in first
For personal use only.
vaginal deliveries in our hospital in the previous years (the
study includes deliveries from 1988).
Previous studies have found prior PPH to be a risk factor
(2.2–3.3 times higher) for recurrent PPH, compared to women
with no history of PPH [24–27]. In the present study a
considerable risk of recurrence of PPH in subsequent
singleton pregnancies after a first vaginal delivery was
observed. In addition to increased risk for recurrent PPH,
women who had PPH in their first delivery were more likely
to undergo CS in their second delivery, which is a novel
finding of our study. Nonetheless, placental abnormalities, in
addition to late adverse outcome of management of the first
PPH, are a well-established risk factor for PPH. Placental
abnormalities are often an indication for CS delivery which
may affect the interpretation of these results [32].
Our study offers several strengths. All deliveries occurred
at the tertiary medical center, which provide access to a
large longitudinal population-based database that has been
validated for its accuracy and reporting reliability. The
pregnancy information was obtained prospectively.
Furthermore, data were reported by an obstetrician directly
after delivery and skilled medical secretaries routinely
reviewed the information prior to entering it into the
database, thereby minimizing recall bias. However, our
study has several inherent weaknesses, mostly due to its
retrospective design, including the potential for missing data.
Another limitation of our study is the lack of an adequate
and accurate gold-standard measurement of postpartum
hemorrhage after vaginal delivery. As a result, visual
estimation of blood loss may lead to underestimation and
misdiagnosed PPH.
In summary, the most important finding of this study is the
remarkable risk for recurrent PPH in subsequent delivery after
Risk factors for postpartum hemorrhage 5
a previous PPH. Furthermore, post-term pregnancies, previ-
ous to first pregnancy fertility treatments, hypertensive
disorders, NPL stage 2 and perineal tears were found to be
independent risk factors for PPH in first vaginal delivery.
Despite these findings and well-established risk factors in the
literature, most cases of PPH have no identifiable risk factors.
The importance of PPH as one of the major causes of
maternal morbidity and mortality, and the increased risk of
recurrence, possess the need of reducing PPH as one of the
main goals of modern obstetrics. This study strengthens the
need for a comprehensive evaluation of prior PPH as a major
risk factor for PPH recurrence.
Acknowledgements
We would like to thank Dr Lena Novack for her great
assistance in the statistical analysis of this study.
Declaration of interest
The authors report no conflicts of interest. The
authors alone are responsible for the content and writing of
this article.
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