Chin Med J 2014;127 (5)

900

Original article
Risk factors associated with emergency peripartum hysterectomy
Jin Rong, Guo Yuna and Chen Yan
Keywords: emergency peripartum hysterectomy; postpartumhemorrhage; placenta accrete; previous cesarean delivery;
tocolytic
Background Use of an emergency peripartum hysterectomy (EPH) as a lifesaving measure to manage intractable
postpartum hemorrhage (PPH) appears to be increasing recently around the world, and the indications for EPH have
changed. The object of this study is to identify risk factors associated with EPH.
Methods We conducted a case-control study of 21 patients who underwent EPH because of intractable PPH between
January 1, 2005 and June 30, 2013, at the International Peace Maternity and Child Health Hospital Shanghai Jiao Tong
University, School of Medicine (IPMCH). The parametric t-test, chi-square tests and Logistic regression models were used
for analysis to identify the risk factors. The results were considered statistically signicant when P<0.05.
Results There were 89178 deliveries during the study period. Twenty-one women had an EPH, with an incidence of
24 per 100000 deliveries. The loss of blood during postpartum hemorrhage of the EPH group was (5 060.73 032.6)
ml, and that of the control group was (2040.8723.5) ml. There was a significant difference of PHH between the
EHP group and the control group (P=0.001). Independent risk factors for EPH from a logistic regression model were:
disseminated intravascular coagulation (DIC) (OR: 9.9, 95% CI 2.834, P=0.003), previous cesarean section (OR: 5.27;
95% CI: 1.4817.9, P=0.009), placenta previa (OR: 6.9; 95% CI 1.62.9, P=0.008), the loss of PPH (OR: 1.001; 95% CI
1.0011.002, P=0.002), placenta accreta (OR: 68; 95% CI 10456, P=0.004), the use of tocolytic agents prenatally (OR:
6.55, 95%CI 1.3432.1,P=0.049), and fetal macrosomia (OR: 6.9, 95% CI 1.2538, P=0.049).
Conclusion Significant risk factors of EPH are DIC, placenta previa, PPH, previous cesarean delivery, and placenta
accrete, the use of tocolytic agents prenatally, and fetal macrosomia.
Chin Med J 2014;127 (5): 900-904

mergency peripartum hysterectomy (EPH) has

been performed as a lifesaving measure to manage
intractable postpartum hemorrhage (PPH). In modern
obstetrics, PPH remains a significant cause of maternal
morbidity and mortality, and the overall incidence is
approximately 5%. 1,2 However, EPH appears to be
increasing by 0.026% in high-income countries and 0.28%
in low income countries,3 1 and the indications for EPH
have changed throughout the years. In an earlier report,4
the major indications for EPH were uterine rupture and
atony. Currently, the increase in the cesarean delivery rate
and the associated risk of abnormal placentation (such as
placenta previa and placenta accreta) have been recognized
as precipitating risk factors for EPH. The aim of the present
study was to determine the demographic characteristics of
patients and risk factors associated with EPH over the last
eight years
METHODS
Patient selection
The study was approved by the Ethics Review Board at the
International Peace Maternity and Child Health Hospital,
Shanghai Jiao Tong University, School of Medicine
(IPMCH). The eligibility criteria for the current study
included; women had the regular prenatal care and delivery
at IPMCH between January 2005 and June 2013. We
retrospectively analyzed all cases (n=21) of EPH during the
study period. The control group included severe postpartum

hemorrhage cases (n=69) with blood loss greater than 1500

ml who were seen during the same period. The data were
collected from the patients IPMCH medical records.
Maternal and neonate demographic data (such as age
and birth weight), medical history including gestational
age, gravidity, parity, premature delivery, multiple
pregnancy, and the use of tocolytic agents prenatally were
assessed. Previous history of infertility, cesarean section,
endometriosis, myoma-enucleation, and hysteroscope,
the types of delivery, the blood loss of postpartum
hemorrhage, and the length of stay (days) at the hospital
after delivery were determined. The perpartum maternal
and fetal complications such as gestational diabetes
mellitus (GDM), preeclampsia, placenta previa, placenta
accrete, polyhydramnios, oligoamnios, placental abruption,
uterine inertia, premature rupture of membrane, rupture of
uterus, macrosomia, still birth, and neonatal asphyxia were
evaluated. The operative complications, including of shock,
disseminated intravascular coagulation (DIC), heart failure,
injury of bladder, intestinal obstruction, poor healing of
DOI: 10.3760/cma.j.issn.0366-6999.20132023
Department of Obstetrics, International Peace Maternity and Child
Health Hospital, Shanghai Jiao Tong University, School of Medicine,
Shanghai 200030, China (Jin R, Guo YN and Chen Y)
Correspondence to: Chen Yan, Department of Obstetrics,
International Peace Maternity and Child Health Hospital, Shanghai
Jiao Tong University, School of Medicine, Shanghai 200030, China
(Tel and Fax: 86-21-64070434. Email: drchenyixin@hotmail.com)

Chinese Medical Journal 2014;127 (5)

901

incision, intrauterine infection, fever after delivery, and the

operative procedures, including uterine artery embolization,
intrauterine packing with gauze, ligation of the ascending
branch of the uterine artery, uterine tamponade of the
bladder, clamping the lower uterine segment, and B-lynch
suture were also evaluated.
Statistical analysis
Statistical analysis was conducted using SPSS version 19.0
(SPSS Inc., Chicago, USA). We conducted preliminary
screening for the potential risk factors between groups:
in detail, the parametric t-test was used to analyze of
continuous variables and chi-square tests were used for
categorical variables. We used the parametric t-test to
analyze the association between emergency peripartum
hysterectomy and the loss of blood during postpartum
hemorrhage. In order to explore the similarity of etiology
for postpartum hemorrhage and emergency peripartum
hysterectomy, we separated the loss of postpartum
hemorrhage into high and low volumes (<3000 ml and
3000 ml). Then logistic regression models were used to
investigate the association between potential risk factors
and the loss of blood during postpartum hemorrhage, and
also the association between potential risk factors and
emergency peripartum hysterectomy. Control variables
included age, gestational weeks, and parity for the both
emergency peripartum hysterectomy and the loss of blood
during postpartum hemorrhage. The results were considered
statistically signicant when P<0.05.
RESULTS
Incidence of EPH
Over the 8-year period between January 2005 and June
2013, 89178 women delivered babies, and among them
1028 (1.15%) women had a PPH, and 21 (0.024%) women
had an EPH. The incidence of EPH was 0.24 per 1 000
deliveries. Cesarean delivery was performed in 44553
(49.96%) women and 21 (0.047%) of these had an EPH.
Demographic and clinical characteristics
The demographic and clinical characteristics of the study
population are shown in Table 1 and Figure 1. The mean age
of EPH patients was (35.1004.146) years old with a range
of 3247 years old, the mean gravidity was 3.7602.071
(range 19), the mean parity was 1.810.62 (range 13),
and the mean gestational age was (36.2382.119) weeks
(range 3441weeks). In EPH cases, the mean length of stay
at the hospital after delivery was (9.8605.141) days (range
520 days), the mean loss of blood during postpartum
hemorrhage was (5060.7603132.624) ml (range
1 00015966 ml). Cesarean section was the route of
delivery in all (100%) EPH cases. Previous cesarean
section (two or more) were conducted in 11 (52.38%) cases,
and complicating central placenta previa in eight (72.73%)
cases. And other indications of cesarean section in the EPH
group included four cases of fetal distress (19.05%), four
cases of antepartum hemorrhage (19.05%), and one case
each of placental abruption and macrosomia (1 case each,

Figure 1. Comparison of risk factors between EPH group and

control group. The column height reflected the occurrence
frequency for each factor, in 21 cases and 69 controls
respectively. Through Chi-square analysis, we found that 11
factors in all playing a role in EPH, comprised of previous
cesarean section, placenta previa, placenta accrete, rupture of
uterus, use Tocolytic agents prenatal, cesarean section, ligation
for ascending branch of uterine artery, shock, DIC, injury of
bladder, neonatal asphyxia.*P<0.05; P<0.01.

Chin Med J 2014;127 (5)

902
Table 1. Measurement analysis of variances
Characteristics
Age (years)
Gravidity
Parity
Gestational age(week)
The length of stay at the hospital after delivery (days)
The loss of postpartum hemorrhage (ml)
The time postpartum hemorrhage (hours)
Birth weight (g)

EPH (n=21)
35.1004.146
3.7602.071
1.8100.62
36.2382.119
9.8605.141
5060 7603132.624
0.3811.359
2891.000745.049

Non-EPH (n=69)
32.1204.858
2.3501.315
1.3900.647
37.7102.184
7.3904.694
2140.800723.574
1.7394.391
3140.840578.760

P values
0.522
0.000*
0.010*
0.008*
0.042*
0.000*
0.167
0.110

The results were showed by meanstandard deviation (SD). *P<0.05.

4.76%).
Difference of PPH between EHP group and the
control group
As shown in Figure 2, the loss of blood during postpartum
hemorrhage in the EHP group was (5060.73032.6) ml,
the loss of blood during postpartum hemorrhage of the EHP
group was (2040.8723.5) ml. There was a significant
difference of blood loss due to PPH between the EHP group
and the control group (P=0.001). The results indicated that

PPH was an important indication for EPH, and PPH to

some extent accounted for EHP.
Logistic regression analysis of risk factors for PPH and
EHP
Table 2 shows the results of the logistic regression analysis
of risk factors for PPH and EPH. The loss of blood
during PPH, previous cesarean section, placenta previa,
placenta accreta, DIC, the use prenatal tocolytic agents,
and macrosomia were associated with an increased risk of
EPH, with OR of 1.001 (1.0011.002), 5.27 (1.4817.9),
6.9 (1.629), 68 (10456), 9.9 (2.834.0), 6.55(1.3432.1),
and 6.9 (1.2538.0), respectively. Moreover, previous
cesarean section, placenta previa, placenta accrete, and DIC
also act as risk factors for PPH with OR 23.8 (3.9144.0),
5.4 (1.518.6), 18.5 (3.889.5), and 36.7 (7.3183.9),
respectively. The results indicated that previous cesarean
section, placenta previa, placenta accrete, and DIC induced
PHH and eventually contributed to EPH. Other risk factors,
such as the loss of PPH, use of prenatal tocolytic agents,
and macrosomia, although unlikely to increase postpartum
hemorrhage, were also indications for EPH.
DISCUSSION

Figure 2. Comparison of PPH between EPH group and control

group. The loss of postpartum hemorrhage of EHP group was
(5060.73032.6) ml, the loss of postpartum hemorrhage of
EHP group was (2040.8723.5) ml. Parametric t-test analysis
indicated that the difference of PPH between EHP group and the
control group was significant (P=0.001).

EPH, although it is actually rare in modern obstetrics,

remains a life saving procedure in cases of severe
hemorrhage.6 The incidence of EPH varies from 41 to 155
per 100000 deliveries in previous reports.7,8 In Cameroon,
the incidence was reported of 125 per 100000 deliveries,
between 1998 and 2008.9 The rate for Nigeria, in a tertiary
institution in a developing country, was 400 per 100000
deliveries between June 1, 2003 and May 31, 2008.10 In
Taiwan, China, an analysis of the National Health Insurance

Table 2. Logistic regression analysis of risk factors for PPH and EPH
Items
Previous cesarean section
Using tocolytic agents prenatal
GDM
Placenta previa
Placenta accreta
Placental abruption
DIC
Macrosomia
Uterine artery embolization
Intrauterine packing with gauze,
Ligation for ascending branch of uterine artery
B-lynch suture

PPH
OR (95% CI)
23.8 (3.9144.0)
2.5 (0.512.5)
0.3 (0.032.6)
5.4 (1.518.6)
18.5 (3.889.5)
1.3 (0.115.4)
36.7 ( 7.3183.9)
4.0 (0.742.8)
1.0 (0.14.2)
3.0 (0.99.0)
7.9 (1.251.7)
34.1 (4.8241.0)

P values
0.001
0.26
0.28
0.001
0.001
0.86
0.001
0.12
0.9
0.052
0.03
0.001

EPH
OR (95% CI)
5.27 (1.4817.9)
6.55 (1.3432.1)
1.09 (0.171.69)
6.9 (1.629)
68 (10456)
1.34 (0.117.1)
9.9 (2.834)
6.9 (1.2538)
2.85 (0.238)
1.0 (0.33.3)
4.2 (0.822)
3.0 (0.713)

P values
0.009
0.049
0.002
0.008
0.004
0.82
0.003
0.049
0.61
0.99
0.15
0.21

Control variables includes age, gestational weeks and parity. The loss of postpartum hemorrhage was separated into high and low level by 3 000 ml.

Chinese Medical Journal 2014;127 (5)

(NHI) database showed the peripartum hysterectomy

rate of 130 per 100000 deliveries in 2002.11 In Sichuan
province, China, the incidence was 190 per 100000 during
the period 20092010. In the present study, the incidence
of EPH was 24 per 100000 deliveries, and this incidence
is far below that in the literature.7,8 All cases that underwent
EPH survived. There are considerable differences in the
incidence in different parts of the world depending on
implication of modern obstetric services: for example,
the use of synthesis operative procedures to prevent
deterioration of PPH, such as uterine artery embolization,
intrauterine packing with gauze, ligation of the ascending
branch of the uterine artery, uterine tamponade bladders,
and B-lynch suture. In addition there are differences
in standards and awareness of antenatal care, and the
effectiveness of family planning activities of a given
community.12 In our study, the mean parity was 1.810.62,
that means the overwhelming majority was primipara and
the risk of repeat caesarean section closely related to EPH
was greatly reduced. This may affect the number of the
incidence of EPH. There is certain of institutions specificity
in data statistics and it is not representativeof all the people.
It is necessary to get a typical result based on a multicenter
study and data analysis.
Because of the increasing use of cesarean section and the
concomitant rise in placenta previa and placenta accrete,13
the incidence of emergency peripartum hysterectomy is
rising in many countries. In the United States, an analysis
based on the US nationwide sample, showed an increase in
the rate of peripartum hysterectomy from 72 per 100000
deliveries in 19941995 to 83 per 100000 deliveries in
20062007.14 The same study showed the leading indication
for EPH in the USA were abnormal placentation including
placenta previa and accreta and PPH from atony. A study in
Egypt15 reported that the incidence of EPH due to uterine
atony has declined from 42% to 29.2% and the incidence
due to abnormal placentation increased from 25.6% to
41.7%. This may be due to the increased rate of placental
accreta associated with an increased number of cesarean
deliveries and better treatment of uterine atony with
prostaglandin preparations during the last two decades.16
From reports from Cameroon9 and Turkey,12 the common
indications for EPH were uterine rupture and uterine
atony.9 The most frequent indication in our study was
PPH associated placenta previa (18/21, 85.71%) including
placenta accreta (16/21, 76.19%), followed by ruptured
uterus (2/21, 9.52%). It seems that massive hemorrhage
due to placental factors is high in developed countries and
conversely, uterine atony is the most common cause of PPH
for EPH in developing or underdeveloped countries.
In our study, the cesarean section rate was 49.96% in the
past eight years; that is one of the highest in the world.
From the literature, the average rate of cesarean section in
mainland Chinese was 46.2% during the period of 2007
2008,17 considerably higher than that reported in other
Asian areas, including India (17.8%), Vietnam (35.6%),
Japan (19.8%),18 and Taiwan (32-34%).11 The cesarean

903

delivery rate in the Unite State was 33% during the period
from 19942007,14 and at the Mayday Hospital, UK it had
risen from 16% in 1989 to 18% in 1998 and 23% in 2008.19
In recent years, because of advance surgical skills and
anesthetic facilities, almost all people believe undergoing a
cesarean section is a no risk, no pain and quick surgery, and
the selective cesarean section has become the first choice of
the majority of pregnant Chinese women. To some extent,
the high rate is due to the low proportion of analgesia labor
and one-child family planning policy. All EPH cases in our
study were performed after cesarean deliveries, but none
was selective cesarean section.
Compared with vaginal delivery, cesarean delivery has
been shown to be associated with higher maternal and
neonatal complications and healthcare costs. In addition,
studies have reported that cesarean delivery is associated
with an increased risk for EPH.14,20 This may be a result
of the associated risk factors for cesarean delivery such as
placenta previa, placenta accreta, or dystocia. Selo-Ojeme et
al21 demonstrated that cesarean delivery was an independent
risk factor for EPH. Nevertheless, in the present study,
it is not cesarean section but previous cesarean section
that was an independent risk factor for EPH and PPH. In
modern obstetrics, due to perfection of surgical skills and
anesthesia, and comprehensive perioperative assessment
and nursing, primary cesarean section has become a lowrisk surgery. However, in a subsequent pregnancy, the
previous cesarean section may have changed normal
anatomy, which increased the risk of placenta previa,
placenta accreta, dystocia and surgical injury, therefore,
increased the incidence of EPH. The safety of vaginal birth
after cesarean delivery (VBAC) remains controversial,
yet the risks were much greater in women who attempted
VBAC and failed. The VBAC rate has decreased markedly
in the United States in recent years.11 Only one EPH case in
the present study who underwent EPH because a ruptured
uterus failed to VBAC. The present analysis does not
calculate VBAC as a risk factor for EPH. However, women
and their prenatal care providers should assess the risks and
benefits rigorously at different stages of pregnancy when
they plan to try VBAC.
In the present study, the use of prenatal tocolytic agents, a
previously undocumented factor, was an independent risk
factor for EPH (OR 6.55 (1.3432.1), P=0.049), but not for
PPH (OR 2.5 (0.512.5), P=0.26). It is obvious that EPH
and PPH are not parallel indicators. For a patient, deciding
on EPH requires comprehending many factors, not just
consideration of the amount of PPH. With an increased
incidence of placenta previa and placenta accrete, tocolytics
with various mechanisms of action such as ritodrine (Anpo),
magnesium sulfate, and oxytocin inhibitors (Atosiban),
have been used to treat vaginal bleeding due to placenta
previa in middle and terminal pregnancy. A substantial
proportion of cases of placenta previa need emergency
surgery because of antenatal bleeding, and there is no time
to stop using the tocolytics before surgery. However, from
our study, we were unable to draw conclusions as to when

Chin Med J 2014;127 (5)

904

is the proper time to stop using tocolytic agents before

surgery. This determination will require collecting more
cases for further research.
In conclusion, the present study has demonstrated that
placenta accrete, DIC, placenta previa, using prenatal
tocolytic agents, PPH, previous cesarean delivery, and fetal
macrosomia are significant risk factors for EPH.
REFERENCES
1. Yang MJ, Wang PH. Peripartum hysterectomy risk factors in
Taiwan. J Chin Med Assoc 2010; 73: 399-400.
2. Park EH, Sachs BP. Postpartum haemorrhage and other
problems of third stage. In: James DK, Steer PJ, Weiner CP,
Gonik B, eds. High Risk PregnancyManagement Options, 2nd
ed. Philadelphia: W.B. Saunders; 1999: 1231-1246.
3. Yucel O, Ozdemir I, Yucel N, Somunkiran A. Emergency
peripartum hysterectomy:a 9 year review. Arch Gynecol Obstet
2006; 274: 84-87.
4. Chestnut DH, Eden, RD, Gall SA, Parker RT. Peripartum
hysterectomy: a review of cesarean and postpartum
hysterectomy. Obstet Gynecol 1985; 65: 365-370.
5. Bai SW, Lee HJ, Cho JS, Park YW, Kim SK, Park KH.
Peripartum hysterectomy and associated factors. J Reprod Med
2003; 48: 148-152.
6. Shellhaas CS, Gilbert S, Landon MB. The frequency and
complication rates of hysterectomy accompanying cesarean
delivery. Obstet Gynecol 2009; 114: 224.
7. Sheiner E, Levy A, Katz M, Mazor M. Identifying risk factors
for peripartum cesarean hysterectomy: a population-based study.
J Reprod Med 2003; 48: 622-666.
8. Kacmar J, Bhimani L, Boyd M, Shah-Hosseini R, Peipert J.
Route of delivery as a risk factor for emergent peripartum
hysterectomy: a case-control study. Obstet Gynecol 2003; 102:
141-145.
9. Tebeu PM, Ndive PE, Ako WT, Biyaga JN. Fomulu emergency
obstetric hysterectomy at university hospital. Int Fed Gynecol
Obstet2013; 105: 91-92.

10. Omole-Ohonsi A, Olayinka HT. Emergencyperipartumhysterec

tomyin a developing country J Obstet Gynaecol Can 2012; 34:
954-960.
11. Jou HJ, Hung HW, Ling PY, Chen SM, Wu SC. Peripartum
hysterectomy in Taiwan. Int J Gynecol Obstet2008; 101: 269272.
12. Yalinkaya A, Gzel AI, Kangal K. Emergency peripartum
hysterectomy: 16-year experience of a medical hospital. J Chin
Med Assoc2010; 73: 360-363.
13. Silver RM, Landon MB, Rouse DJ. Maternal morbidity
associated with multiple repeat cesarean deliveries. Obstet
Gynecol 2006; 107: 1226-1232.
14. Bateman BT, Mhyre JM, Callaghan WM, Kuklina EV.
Peripartumhysterectomyin theUnited States: nationwide 14
year experience. Am J Obstet Gynecol 2012; 63. e1-e8.
15. Bashir A, Ashraf R, Gul A, Tajamul A. Peripartum hysterectomy.
Ann King Edward Coll 2007; 13: 111-112.
16. Mesbah Y, Ragab A, Fialla E, Barakat R, Badawy A, et al.
Emergency peripartum hysterectomy: the experience of a tertiary
referral hospital. Middle East Fertil Soc J 2013; 18: 89-93.
17. Liang J, Zhu J, Dai L, Li X, Li M, Wang Y. Maternal mortality
in China, 19962005. Int J Gynecol Obstet 2010; 110: 93-96.
18. Lumbiganon P, Laopaiboon M, Glmezoglu AM, Souza JP,
Taneepanichskul S, Ruyan P, et al. Method of delivery and
pregnancy outcomes in Asia: the WHO global survey on
maternal and perinatal health 200708. Lancet 2010; 375: 490499.
19. Lone F, Sultan AH, Thakar R, Beggs A. Risk factors and
management patterns for emergency obstetric hysterectomy over
2 decades. Int J Gynecol Obstet2010; 109: 12-15.
20. Bodelon C, Bernabe-Ortiz A, Schiff MA, Reed SD. Factors
associated with peripartum hysterectomy. Obstet Gynecol 2009;
114: 115-123.
21. Selo-Ojeme DO, Bhattacharjee P, Izuwa-Njoku NF, Kadir
RA. Emergency peripartum hysterectomy in a tertiary London
hospital. Arch Gynecol Obstet 2005; 271: 154-159.

(Received September 1, 2013)

Edited by Chen Limin