Anda di halaman 1dari 6

International Journal of Gynecology and Obstetrics 134 (2016) 202207

Contents lists available at ScienceDirect

International Journal of Gynecology and Obstetrics


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

CLINICAL ARTICLE

Incorporating uterine artery embolization in the treatment of cesarean


scar pregnancy following diagnostic ultrasonography
Yang Li a, Weiwen Wang b, Ting Yang a, Xing Wei a, Xiaofeng Yang a,
a
b

Department of Gynecology and Obstetrics, First Afliated Hospital, Xi'an Jiaotong University, Xi'an, China
Department of Neurosurgery, Tangdu Hospital, Fourth Military Medical University, Xi'an, China

a r t i c l e

i n f o

Article history:
Received 5 September 2015
Received in revised form 16 December 2015
Accepted 24 March 2016
Keywords:
Cesarean scar pregnancy
Ultrasonographic pattern
Uterine artery embolization

a b s t r a c t
Objective: To evaluate combining uterine artery embolization (UAE) with other treatments for cesarean scar
pregnancy (CSP). Methods: A retrospective study included patients attending the First afliated Hospital of
Xi'an Jiaotong University, China, between March 1, 2009 and March 31, 2014, who were diagnosed with CSP.
Patients were classied by ultrasonography as having endogenous CSP (CSP type I [CSP-I]) or exogenous CSP
(CSP type II [CSP-II]). Patient outcomes were compared between patients who underwent treatment that
included or excluded UAE. Patient records were reviewed and patients were interviewed by telephone to report
on recovery following treatment. Results: In total, 52 patients met the inclusion criteria. In patients with CSP-I, the
blood loss, length of hospital stay, and time before restoration of normal human chorionic gonadotropin levels
were signicantly higher in patients who were treated with methotrexate combined with dilatation and curettage compared with those treated with UAE combined with dilatation and curettage (P b 0.05). In patients
with CSP-II, blood loss was lower in patients treated with UAE combined with excision compared with excision
alone (P b 0.001). Conclusion: Incorporating UAE in the treatment of CSP-I and CSP-II was safe; CSP should be
properly classied to select the appropriate treatment.
2016 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. This is
an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction
Cesarean scar pregnancy (CSP) is a term that describes the implantation of a gestational sac at the site of a previous cesarean delivery scar
and was rst described by Larsen and Solomon in 1978 [1]. The incidence of CSP has been reported to be one case per 18002216 normal
pregnancies; this rate could rise in the future owing to increasing
rates of cesarean deliveries [24]. Links have been suggested between
uterine scar dehiscence or small-scar defects after cesarean deliveries
and later CSPs [5], and routine transvaginal ultrasonography has been
recommended in early pregnancy for patients who have previously undergone a cesarean delivery [6]. Vial et al. [7] classied CSP based on
transvaginal ultrasonography. Endogenous CSP (CSP type I [CSP-I]) is
caused by the implantation of the amniotic sac at the cesarean-scar
site followed by progression towards either the cervical isthmic space
or the uterine cavity. Exogenous CSP (CSP type II [CSP-II]) results from
the deep implantation of the amniotic sac into a previous cesarean
scar defect with growth that inltrates the uterine myometrium,

Corresponding author at: Department of Gynecology and Obstetrics, First


Afliated Hospital, Xi'an Jiaotong University, 277 West Yanta Road, Xi'an 710061,
China. Tel.: + 86 186 0290 0810.
E-mail address: yxf73@163.com (X. Yang).

creating a bulge from the uterine serosal layer. The use of ultrasonography in clinical practice to assess the risks posed by CSP has been demonstrated [8,9] and this approach is widely applied in China.
Complications encountered in the treatment of CSP make it clinically
challenging. Initially, mifepristone is administered or curettage is
performed to terminate pregnancy; however, CSP is often accompanied
by repeated vaginal bleeding, abnormal beta human chorionic gonadotropin (-hCG) levels, and the growth of CSP masses. Moreover, deep
implantation in CSP-II can lead to uncontrollable hemorrhaging if highly
vascularized tissues are dissected from the uterus. Consequently, in recent years, considerable attention has focused on different methods
for managing CSP to improve patient outcomes. Protocols for the treatment of CSP that have been investigated include methotrexate (MTX)
injection (systemic or local), dilatation and curettage, uterine artery
embolization (UAE), the excision of CSP lesions via laparotomy, and
laparoscopic or hysteroscopic surgery; these approaches aim to prevent
hemorrhage and preserve fecundity [1016]. The benets of including
UAE in the treatment of CSP have been demonstrated previously [8,16,
17]. Despite UAE having been proven to be a viable intervention to
control hemorrhaging and preserve the uterus, there is no consensus
on optimal combination therapies for each CSP type.
The aim of the present study was to analyze patient outcomes and
complications following the use of UAE in the treatment of patients
with CSP.

http://dx.doi.org/10.1016/j.ijgo.2015.12.006
0020-7292/ 2016 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Y. Li et al. / International Journal of Gynecology and Obstetrics 134 (2016) 202207

2. Materials and methods


The present retrospective study analyzed data from patients who
were diagnosed and treated for CSP at the First afliated Hospital of
Xi'an Jiaotong University, China, between March 1, 2009 and March
31, 2014. CSP was conrmed by a history of a prior cesarean delivery,
clinical symptoms (postmenstrual spotting, mild lower abdominal
pain), ultrasonography examination, and serum -hCG levels. Patients
were eligible for inclusion in the study if they met the following criteria
under ultrasonography examination: (1) empty uterus and cervical
canal; (2) development of the gestational sac or identication of a
mixed-echo mass in the anterior part of the cesarean scar; (3) very
thin myometrium or an absence of healthy myometrium between the
bladder wall and the sac/mass or when running through the amniotic
sac; and (4) the gestational sac or mixed-echo mass being located
toward either the cervical isthmic space or the uterine cavity in CSP-I,
or the inltration of the gestational sac or mixed-echo mass into the
myometrium and/or forming a bulge from the uterine serosal layer in
CSP-II. Ultrasonography ndings were used in guiding physician decisions on patient treatments. Patients with CSP-I meeting the above
criteria were eligible for inclusion if they had been treated with either
MTX followed by dilatation and curettage, or UAE followed by dilatation
and curettage. Data from patients with CSP-II were included in the
present study if they had been treated through direct excision of the
CSP lesion using laparotomy or if they received UAE treatment followed
by CSP lesion excision by laparotomy. The present study was approved
by the Institutional Review Board of Xi'an Jiaotong University; obtaining
informed consent from patients for the use of medical record data was
waived owing to the retrospective nature of the study and all patients
provided verbal consent to participate in telephone interviews.
Patients who underwent treatment for CSP-I with MTX received an
intramuscular MTX injection (50 mg/m2; Shanxi Powerdone
Pharmaceutics Co Ltd., Datong, China). Patients were then evaluated
after 1 week; if a patient's serum -hCG level had decreased by at
least 50%, or to below 2000 mIU/mL, follow-up ultrasonography
examinations were performed to evaluate chorionic sac volume and
vascularization. If initial MTX treatment was ineffective, patients received a further dose and follow-up period. If follow-up ultrasonography revealed no growth in CSP masses, dilatation and curettage was
performed with abdominal ultrasonography monitoring.
When UAE was included in the treatment of patients who had CSP-I,
the uterine artery was selectively catheterized using a Rosch hepatic
catheter (Terumo Corporation, Tokyo, Japan) and was embolized using

203

gel foam sponge particles (9001200 m). Embolization proceeded


until the lower uterine segment was completely occluded. Digital subtraction angiography images were acquired during the procedure
(Philips FD20; Philips, Best, The Netherlands). Dilatation and curettage
with ultrasonography monitoring was performed 16 h to remove CSP
lesions completely. Patients' right lower extremities were immobilized
for 12 h after embolization, and patient pulses were measured at the
dorsalis pedis artery every hour. Patients were monitored for the
occurrence of vascular complications for 72 h.
Patients with CSP-II underwent the direct excision of CSP lesions via
laparotomy with or without UAE. If the anatomical relationship was
clear, the bladder peritoneum was incised and pressure was applied to
the bladder to access the lower uterine segment and upper cervical
segment. Following this, the gestational tissue, blood clots, and
myometrial scar were removed. Wound repair was performed with
interrupted sutures in the myometrium and a continuous suture in
the serosal layer. When UAE was included in the treatment protocol
for patients with CSP-II, it was performed as described in patients
with CSP-I, with direct excision following after 16 h. All patients with
CSP-II received general anesthesia during excision operations and lesion
tissues excised from patients with CSP-II underwent pathological
examination to conrm the preoperative ultrasonography diagnosis.
Data were collected from patients' medical records and operation
notes. Treatment protocols and post-operation data up to the normalization of serum -hCG levels were retrieved for each patient. Patients
were contact by telephone and information was collected on the time
taken after treatment to resume menstruation, on any anomalous
symptoms experienced, and of any subsequent pregnancies.
Statistical analyses were performed using SPSS version 20.0 (IBM,
Armonk, NY, USA). Clinical data, including age, gravidity and parity,
the time interval between the previous cesarean delivery and the
diagnosis of CSP, the duration of follow-up after treatment for CSP,
intraoperative blood loss, and the length of hospital stay during
treatment, were expressed as the mean SD or as the median and
interquartile range. The MannWhitney U test was used to compare
the differences between patients receiving different treatments and
P b 0.05 was considered statistically signicant.
3. Results
During the 6-year study period, the CSP to normal pregnancy ratio at
the study institution was 57:16,391. Of these 57 patients, 25 (44%) were
classied as CSP-I and 32 (56%) were classied as CSP-II (Fig. 1). The age

Fig. 1. Transvaginal ultrasonography images. (a) A 30-year-old woman with cesarean scar pregnancy type I; a gestational sac is embedded at the site of a previous cesarean scar. (b) A 29year-old woman with cesarean scar pregnancy type II; the gestational sac had implanted into a previous cesarean scar defect with growth that has inltrated into the uterine myometrium
and bulges from the uterine serosal surface.

204

Y. Li et al. / International Journal of Gynecology and Obstetrics 134 (2016) 202207

Table 1
Clinical characteristics of patients with CSP at baseline.a
Characteristic

CSP-I (n = 24)

CSP-II (n = 28)

P valueb

Age, y
Duration of gestation at diagnosis, d
Gravidity
Parity
Time between previous cesarean delivery and index pregnancy, y
Pretreatment serum -hCG, mIU/mL

31.0 (29.035.0)
51 (41.362.8)
3 (24)
1 (11)
4.1 2.3
5458.5 (2277.323,259.8)

30.5 (27.335.0)
59.5 (52.380.5)
3 (34)
1 (11)
7.0 6.3
3641.0 (1029.811,404.5)

0.467
0.017
0.209
0.571

Abbreviations: CSP, cesarean scar pregnancy; CSP-I, cesarean scar pregnancy type I; CSP-II, cesarean scar pregnancy type II; -hCG, beta human chorionic gonadotropin.
a
Values are given as mean SD or median (interquartile range), unless indicated otherwise.
b
MannWhitney U test.

range of patients diagnosed with CSP was 2347 years. The duration of
pregnancy at the time of CSP diagnosis was 31112 days. The time
interval between patients' previous caesarean section and the current
CSP ranged from 0.5 years to 23.0 years. Among the 57 patients
experiencing CSP, 53 (93%) had experienced one previous cesarean
delivery, and 4 (7%) had undergone two. Placenta previa during most
recent pregnancy was reported by one patient. The range of serum
-hCG levels recorded among patients was 13.6893,207.00 mIU/
mL. The range of the largest diameter of CSP masses, measured
using ultrasonography, was 1.07.5 cm in patients with CSP-I and
1.07.8 cm in patients with CSP-II. Among the potentially eligible
patients with CSP-I, one patient had been referred to the emergency
department of the study institution with a vaginal-bleeding
emergency. This patient had been treated with MTX but had
experienced a steady increase in serum -hCG levels and an increase
in CSP-mass volume that was visible under ultrasonography
examination; the patient underwent CSP lesion excision by
laparotomy and, consequently, was excluded from the present

study. Among patients with CSP-II, four patients who underwent


CSP lesion excision experienced massive vaginal bleeding
(N1200 mL); these patients received blood transfusions and
underwent emergency ligation of the internal iliac artery. However,
this treatment did not resolve the complications and life-saving
emergency subtotal hysterectomies were performed for all four patients, resulting in their exclusion from the present study. This resulted in 52 patients being included in the present retrospective
study and telephone interviews. The baseline clinical characteristics
of the patients included in the study are presented in Table 1.
Among the patients with CSP-I included in the present study, 14 were
treated with intramuscular MTX injections. The rst injection of MTX was
not effective in one patient. This individual was managed by administering intramuscular MTX (50 mg/m2) again 8 days after initial MTX administration. On day 15, the patient's serum -hCG level was below
2000 mIU/mL and they underwent ultrasonography examination. Ultrasonography examinations revealed no growth in all 14 patients, and
dilatation and curettage with abdominal ultrasonography monitoring

Fig. 2. Digital subtraction angiogram images from a patient with cesarean scar pregnancy type I who was treated using transcatheter uterine arterial embolization.

Y. Li et al. / International Journal of Gynecology and Obstetrics 134 (2016) 202207

205

observed. No UAE-associated adverse effects, including postembolization syndrome and pelvic tissue damage, were observed during hospitalization. Mild lower abdominal pain continuing for several
days was recorded in all patients who underwent UAE; this pain was
controlled successfully with intravenous urbiprofen axetil (Kaifen;
Beijing Tide Pharmaceutical Co, Beijing, China). No necrosis of pelvic
organs, infection, amenorrhea, or premature ovarian failure was
recorded during the study period. During weekly follow-up, serum
-hCG levels steadily decreased without the need for additional
treatment in all patients. Following treatment, the time to normalization of serum -hCG levels was 26 weeks and 25 weeks in patients
with CSP-I and CSP-II, respectively. All of the patients were experiencing
normal menstrual cycles and menstruation volumes without
dysmenorrhoea within 48 weeks of treatment (Table 2, Table 3).
From the telephone interviews conducted, 35 patients reported
using contraception after treatment (22 patients reported using intrauterine devices and 13 patients reported using condoms); at least
2 years of follow-up data was available for these patients. Additionally,
one patient reported a successful natural intrauterine pregnancy that
occurred 20 months after treatment.
4. Discussion

Fig. 3. Cesarean scar lesion tissues from a patient with cesarean scar pregnancy type II were
subjected to pathological examination, conrming the preoperative ultrasonography
diagnosis. The arrows indicate the chorionic villi.

was performed. UAE before dilatation and curettage was performed in


the treatment of 10 patients with CSP-I; digital subtraction angiography
images were obtained from patients during embolization (Fig. 2).
Direct excision of CSP lesions via laparotomy was used to treat 14
patients with CSP-II and UAE was included in the treatment of 14
patients with CSP-II before direct excision of CSP lesions. Tissue
samples from CSP lesions were obtained from patients with CSP-II for
pathological examination (Fig. 3).
No signicant difference was found when comparing the time before
resuming menstruation between the two treatment protocols for
patients with CSP-I (Table 2). However, the intraoperative blood loss
(P b 0.001), length of hospital stay (P = 0.002), and time before normalization of serum -hCG levels (P = 0.026) were signicantly higher in patients treated with MTX prior to dilatation and curettage in comparison
with patients treated with UAE before dilatation and curettage (Table 2).
No signicant difference was recorded in the time before resuming
menstruation, the time before serum -hCG normalization, and the
duration of hospitalization between patients with CSP-II treated with
CSP lesion excision alone and those treated with UAE before lesion
excision. Intraoperative blood loss was lower in patients who underwent
UAE prior to CSP lesion excision (P b 0.001) (Table 3).
During treatment and follow-up, no MTX-related adverse events,
including leukopenia, alopecia, and abnormal liver function, were

The present study examined the treatment outcomes for 52 patients


with CSP over a 6-year period. Classication using ultrasonography
provided the basis for the management of patients. Including UAE in
the treatment of patients with CSP-I resulted in lower levels of
intraoperative blood loss, reduced hospitalization for treatment, and a
reduction in the time taken for serum -hCG levels to normalize compared with using MTX in the treatment of CSP-I. Including UAE before
the direct excision of CSP lesions in CSP-II patients resulted in reduced
intraoperative blood loss.
The accuracy of ultrasonography and magnetic resonance imaging in
diagnosing CSP has been demonstrated previously [5,18,19]. It notable
that magnetic resonance imaging is a costly diagnostic technique and
that this must often be taken into account in clinical environments.
The use of ultrasonography in diagnosing CSP has the advantages of
being non-invasive, simple, and cheap. The level of diagnostic accuracy
in the present study can be attributed to a combination of transvaginal
ultrasonography, a long duration of gestation at the time of diagnosis,
and detailed patient histories. The pathological evaluations performed
in patients with CSP-II in the study conrmed the accuracy of using
ultrasonography for diagnosis.
Considering the severe maternal morbidity that can result from CSP,
including massive hemorrhages, uterine rupture, and the occurrence of
an adherent placenta, the induced abortion of a pregnancy following a
CSP diagnosis is widely accepted [2022]. However, a previous review
of 751 patients with CSP demonstrated that complications, including
hysterectomies, laparotomies, and emergency UAE procedures,
occurred in 331 (44.1%) patients [19]. The aim of classifying CSP prior
to treatment in the present study was to minimize the risk of severe
complications based on the features of different CSP types. In patients
with CSP-I, the intention behind the choice of treatment was to avoid
prolonged procedures, with the aim of reducing complications and

Table 2
Patient outcomes following treatment for CSP-I.a
Variable

Patients treated with methotrexate before dilatation


and curettage (n = 14)

Patients treated with uterine artery embolization before dilatation


and curettage (n = 10)

P valueb

Duration of hospitalization, d
Time before -hCG normalization, wk
Intraoperative blood loss, mL
Time before resuming menstruation, d

8.5 (8.014.3)
3.5 (2.04.0)
200.0 (172.5257.5)
31.0 (29.039.3)

5.5 (4.07.5)
2.0 (1.03.0)
55.0 (30.072.5)
30.5 (29.832.3)

0.002
0.026
b0.001
0.625

Abbreviations: CSP-I, cesarean scar pregnancy type I; -hCG, beta human chorionic gonadotropin.
a
Values are given as median (interquartile range) unless indicated otherwise.
b
MannWhitney U test.

206

Y. Li et al. / International Journal of Gynecology and Obstetrics 134 (2016) 202207

Table 3
Patient outcomes following treatment for CSP-II.a
Variable

Patients treated with direct excision of CSP lesion


(n = 14)

Patients treated with uterine artery embolization direct excision of CSP


lesion (n = 14)

P valueb

Duration of hospitalization, d
Time before -hCG normalization, wk
Intraoperative blood loss, mL
Time before resuming menstruation, d

9.0 (7.810.3)
2.0 (1.03.3)
575.0 (450.0612.5)
34.5 (32.036.3)

8.0 (6.09.0)
2.0 (1.02.0)
265.0 (200.0300.0)
34.5 (31.337.5)

0.150
0.114
b0.001
0.769

Abbreviations: CSP-II, cesarean scar pregnancy type II; CSP, cesarean scar pregnancy; -hCG, beta human chorionic gonadotropin.
a
Values are given as median (interquartile range) unless indicated otherwise.
b
MannWhitney U test.

treatment failures. For patients with CSP-II, the preservation of patient


fertility and a reduction in the risk of massive hemorrhage were priorities. Individualizing treatment according to the different CSP subtypes
resulted insubstantial improvements in clinical outcomes.
Systemic MTX injections, dilatation and curettage, and UAE are
treatments that have all demonstrated high complication rates previously [19]. Consequently, combining therapeutic approaches should be
considered when selecting the treatment options. Combining MTX therapy with suction curettage in the treatment of CSP has been reported to
result in a shorter resolution time for CSP masses and serum -hCG
levels [15]. Moreover, UAE in combination with dilatation and curettage
and MTX, or combined with chemoembolization has been reported to
reduce complication rates [8,12,16,23,24]. In the present study, UAE
was used as an initial intervention for CSP with the aim of controlling
bleeding risks and preserving future fertility. A notable observation
was that although initial -hCG levels, CSP mass diameter, and the presence of fetal heart activity were not considered when making treatment
decisions, the use of UAE prior to further treatment reduced intraoperative blood loss in both CSP-I and CSP-II, and reduced the amount of
time until serum -hCG levels normalized in patients with CSP-I. Consequently, UAE appears to be a simple, safe, and effective intervention in
the treatment of CSP. Although UAE can obstruct local blood ow in
areas around the CSP mass, the gradual re-establishment of circulation
presents a risk for hemorrhage [12]. For this reason, dilatation and curettage or CSP-lesion excision was performed within 16 h of UAE in
the present study; this time interval was shorter than those used in previous studies [8,12,16,23] and did not result in an increase in the duration of hospitalization. This protocol did not affect outcomes or lead to
increased complications; consequently, it is suggested that only a
short interval (16 h) be left after UAE before proceeding with further
treatment. However, a large prospective multicenter study examining
this is still required to guide future clinical approaches.
Including UAE interventions did not change the time before the resumption of menstruation when used in the treatment of either CSP
subtype, which could suggest an advantage for preserving fertility.
Hirakawa et al. [25] reported successful natural intrauterine pregnancies following UAE treatment in three patients. In the present study,
post-treatment contraceptive use was reported by 35 individuals with
at least 2-year follow-up data available. A successful natural intrauterine
pregnancy was reported by only one patient, who was among the CSP-I
cohort. Further assessment of how including UAE in the treatment of
CSP affects fertility outcomes is necessary.
The present study did have some limitations. Owing to the low incidence of CSP, the present study had a small sample size. With increases
in cesarean-delivery rates globally, CSP could become more common
and this could facilitate larger studies in the future. To establish
standardized procedures for the treatment of different CSP subtypes,
future studies need to recruit more patients and use multicenter data
to compare the different treatment modalities used across the different
CSP subtypes.
In conclusion, the management of CSP requires safe and effective
treatment protocols to reduce severe complications. The present study
demonstrated that the use of ultrasonography examination should be
considered to obtain diagnostic information that can be useful in

individualizing patient treatment. Combining UAE with dilatation and


curettage in the treatment of patients with CSP-I patients, and with
CSP-lesion excision in the treatment of patients with CSP-II are effective
treatment options for these CSP subtypes. However, long-term followup and further research are still warranted.

Conicts of interest
The authors have no conicts of interest.

References
[1] Larsen JV, Solomon MH. Pregnancy in a uterine scar sacculusan unusual cause of
postabortal haemorrhage. A case report. S Afr Med J 1978;53(4):1423.
[2] Mi J, Liu F. Rate of caesarean section is alarming in China. Lancet 2014;383(9927):
14634.
[3] Rotas MA, Haberman S, Levgur M. Cesarean scar ectopic pregnancies: etiology,
diagnosis, and management. Obstet Gynecol 2006;107(6):137381.
[4] Vogel JP, Betrn AP, Vindevoghel N, Souza JP, Torloni MR, Zhang J, et al. use of the
Robson classication to assess caesarean section trends in 21 countries: a secondary
analysis of two WHO multicountry surveys. Lancet Glob Health 2015;3(5):e26070.
[5] Peng KW, Lei Z, Xiao TH, Jia FG, Zhong WX, Gao Y, et al. rst trimester caesarean scar
ectopic pregnancy evaluation using MRI. Clin Radiol 2014;69(2):1239.
[6] Zhang Y, Gu Y, Wang JM, Li Y. Analysis of cases with cesarean scar pregnancy. J
Obstet Gynaecol Res 2013;39(1):195202.
[7] Vial Y, Petignat P, Hohlfeld P. Pregnancy in a cesarean scar. Ultrasound Obstet
Gynecol 2000;16(6):5923.
[8] Lian F, Wang Y, Chen W, Li J, Zhan Z, Ye Y, et al. Uterine artery embolization
combined with local methotrexate and systemic methotrexate for treatment of
cesarean scar pregnancy with different ultrasonographic pattern. Cardiovasc
Intervent Radiol 2012;35(2):28691.
[9] Maymon R, Halperin R, Mendlovic S, Schneider D, Vaknin Z, Herman A, et al. ectopic
pregnancies in Caesarean section scars: the 8 year experience of one medical centre.
Hum Reprod 2004;19(2):27884.
[10] Chou YM, Wu D, Wu KY, Lee CL. hysteroscopic removal of cesarean scar pregnancy
after methotrexate treatment failure. Gynecol Minim Invasive Ther 2013;2(2):702.
[11] Kim K, Pietrzak A, Gonzalez S, Podgony K. severe hemorrhage in a rst-trimester
cesarean scar pregnancy during dilation and curettage. Int J Obstet Anesth 2010;
19(3):3489.
[12] Shen L, Tan A, Zhu H, Guo C, Liu D, Huang W. BilatQeral uterine artery
chemoembolization with methotrexate for cesarean scar pregnancy. Am J Obstet
Gynecol 2012;207(5):386.e16.
[13] Timor-Tritsch IE, Monteagudo A, Santos R, Tsymbal T, Pineda G, Arslan AA. The
diagnosis, treatment, and follow-up of cesarean scar pregnancy. Am J Obstet
Gynecol 2012;207(1), 44.e1-13.
[14] Wang HY, Zhang J, Li YN, Wei W, Zhang DW, Lu YQ, et al. Laparoscopic management
or laparoscopy combined with transvaginal management of type II cesarean scar
pregnancy. JSLS 2013;17(2):26372.
[15] Wang JH, Xu KH, Lin J, Xu JY, Wu RJ. Methotrexate therapy for cesarean section scar
pregnancy with and without suction curettage. Fertil Steril 2009;92(4):120813.
[16] Zhang B, Jiang ZB, Huang MS, Guan SH, Zhu KS, Qian JS, et al. Uterine artery embolization combined with methotrexate in the treatment of cesarean scar pregnancy:
results of a case series and review of the literature. J Vasc Interv Radiol 2012;
23(12):15828.
[17] Halperin R, Schneider D, Mendlovic S, Pansky M, Herman A, Maymon R. Uterinepreserving emergency surgery for cesarean scar pregnancies: another medical
solution to an iatrogenic problem. Fertil Steril 2009;91(6):26237.
[18] Chong Y, Zhang K, Zhou Y, Han J, Zhu F, Guo H, et al. Clinical value of MRI in cesarean
scar pregnancy. [in Chinese] Zhonghua Fu Chan Ke Za Zhi 2014;49(12):9148.
[19] Timor-Tritsch IE, Monteagudo A. Unforeseen consequences of the increasing rate of
cesarean deliveries: early placenta accreta and cesarean scar pregnancy. A review.
Am J Obstet Gynecol 2012;207(1):1429.
[20] Timor-Tritsch IE, Monteagudo A, Cali G, Vintzileos A, Viscarello R, Al-Khan A, et al.
Cesarean scar pregnancy is a precursor of morbidly adherent placenta. Ultrasound
Obstet Gynecol 2014;44(3):34653.

Y. Li et al. / International Journal of Gynecology and Obstetrics 134 (2016) 202207


[21] Roberge S, Boutin A, Chaillet N, Moore L, Jastrow N, Demers S, et al. Systematic review of cesarean scar assessment in the nonpregnant state: imaging techniques
and uterine scar defect. Am J Perinatol 2012;29(6):46571.
[22] Dickerhoff LA, Mahal AS, Stockdale CK, Hardy-Fairbanks AJ. Management of cesarean
scar pregnancy in the second trimester: a report of three cases. J Reprod Med 2015;
60(34):1658.
[23] Lan W, Hu D, Li Z, Wang L, Yang W, Hu S. Bilateral uterine artery chemoembolization
combined with dilation and curettage for treatment of cesarean scar pregnancy: A
method for preserving the uterus. J Obstet Gynaecol Res 2013;39(6):11538.

207

[24] Zhuang Y, Huang L. Uterine artery embolization compared with methotrexate for
the management of pregnancy implanted within a cesarean scar. Am J Obstet
Gynecol 2009;201(2):152.e13.
[25] Hirakawa M, Tajima T, Yoshimitsu K, Irie H, Ishigami K, Yahata H, et al. Uterine artery
embolization along with the administration of methotrexate for cervical ectopic pregnancy: technical and clinical outcomes. AJR Am J Roentgenol 2009;192(6):16017.