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International Journal of Gynecology and Obstetrics 134 (2016) 202–207

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International Journal of Gynecology and Obstetrics

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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,⁎
Department of Gynecology and Obstetrics, First Affiliated 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 a b s t r a c t

Article history: Objective: To evaluate combining uterine artery embolization (UAE) with other treatments for cesarean scar
Received 5 September 2015 pregnancy (CSP). Methods: A retrospective study included patients attending the First affiliated Hospital of
Received in revised form 16 December 2015 Xi'an Jiaotong University, China, between March 1, 2009 and March 31, 2014, who were diagnosed with CSP.
Accepted 24 March 2016 Patients were classified 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
Cesarean scar pregnancy
Ultrasonographic pattern
on recovery following treatment. Results: In total, 52 patients met the inclusion criteria. In patients with CSP-I, the
Uterine artery embolization blood loss, length of hospital stay, and time before restoration of normal β human chorionic gonadotropin levels
were significantly higher in patients who were treated with methotrexate combined with dilatation and curet-
tage 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 classified 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 creating a bulge from the uterine serosal layer. The use of ultrasonogra-
phy in clinical practice to assess the risks posed by CSP has been demon-
Cesarean scar pregnancy (CSP) is a term that describes the implanta- strated [8,9] and this approach is widely applied in China.
tion of a gestational sac at the site of a previous cesarean delivery scar Complications encountered in the treatment of CSP make it clinically
and was first described by Larsen and Solomon in 1978 [1]. The inci- challenging. Initially, mifepristone is administered or curettage is
dence of CSP has been reported to be one case per 1800–2216 normal performed to terminate pregnancy; however, CSP is often accompanied
pregnancies; this rate could rise in the future owing to increasing by repeated vaginal bleeding, abnormal beta human chorionic gonado-
rates of cesarean deliveries [2–4]. Links have been suggested between tropin (β-hCG) levels, and the growth of CSP masses. Moreover, deep
uterine scar dehiscence or small-scar defects after cesarean deliveries implantation in CSP-II can lead to uncontrollable hemorrhaging if highly
and later CSPs [5], and routine transvaginal ultrasonography has been vascularized tissues are dissected from the uterus. Consequently, in re-
recommended in early pregnancy for patients who have previously un- cent years, considerable attention has focused on different methods
dergone a cesarean delivery [6]. Vial et al. [7] classified CSP based on for managing CSP to improve patient outcomes. Protocols for the treat-
transvaginal ultrasonography. Endogenous CSP (CSP type I [CSP-I]) is ment of CSP that have been investigated include methotrexate (MTX)
caused by the implantation of the amniotic sac at the cesarean-scar injection (systemic or local), dilatation and curettage, uterine artery
site followed by progression towards either the cervical isthmic space embolization (UAE), the excision of CSP lesions via laparotomy, and
or the uterine cavity. Exogenous CSP (CSP type II [CSP-II]) results from laparoscopic or hysteroscopic surgery; these approaches aim to prevent
the deep implantation of the amniotic sac into a previous cesarean hemorrhage and preserve fecundity [10–16]. The benefits of including
scar defect with growth that infiltrates the uterine myometrium, 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.
⁎ Corresponding author at: Department of Gynecology and Obstetrics, First
Affiliated Hospital, Xi'an Jiaotong University, 277 West Yanta Road, Xi'an 710061,
The aim of the present study was to analyze patient outcomes and
China. Tel.: + 86 186 0290 0810. complications following the use of UAE in the treatment of patients
E-mail address: yxf73@163.com (X. Yang). with CSP.

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
Y. Li et al. / International Journal of Gynecology and Obstetrics 134 (2016) 202–207 203

2. Materials and methods gel foam sponge particles (900–1200 μm). Embolization proceeded
until the lower uterine segment was completely occluded. Digital sub-
The present retrospective study analyzed data from patients who traction angiography images were acquired during the procedure
were diagnosed and treated for CSP at the First affiliated Hospital of (Philips FD20; Philips, Best, The Netherlands). Dilatation and curettage
Xi'an Jiaotong University, China, between March 1, 2009 and March with ultrasonography monitoring was performed 1–6 h to remove CSP
31, 2014. CSP was confirmed by a history of a prior cesarean delivery, lesions completely. Patients' right lower extremities were immobilized
clinical symptoms (postmenstrual spotting, mild lower abdominal for 12 h after embolization, and patient pulses were measured at the
pain), ultrasonography examination, and serum β-hCG levels. Patients dorsalis pedis artery every hour. Patients were monitored for the
were eligible for inclusion in the study if they met the following criteria occurrence of vascular complications for 72 h.
under ultrasonography examination: (1) empty uterus and cervical Patients with CSP-II underwent the direct excision of CSP lesions via
canal; (2) development of the gestational sac or identification of a laparotomy with or without UAE. If the anatomical relationship was
mixed-echo mass in the anterior part of the cesarean scar; (3) very clear, the bladder peritoneum was incised and pressure was applied to
thin myometrium or an absence of healthy myometrium between the the bladder to access the lower uterine segment and upper cervical
bladder wall and the sac/mass or when running through the amniotic segment. Following this, the gestational tissue, blood clots, and
sac; and (4) the gestational sac or mixed-echo mass being located myometrial scar were removed. Wound repair was performed with
toward either the cervical isthmic space or the uterine cavity in CSP-I, interrupted sutures in the myometrium and a continuous suture in
or the infiltration of the gestational sac or mixed-echo mass into the the serosal layer. When UAE was included in the treatment protocol
myometrium and/or forming a bulge from the uterine serosal layer in for patients with CSP-II, it was performed as described in patients
CSP-II. Ultrasonography findings were used in guiding physician deci- with CSP-I, with direct excision following after 1–6 h. All patients with
sions on patient treatments. Patients with CSP-I meeting the above CSP-II received general anesthesia during excision operations and lesion
criteria were eligible for inclusion if they had been treated with either tissues excised from patients with CSP-II underwent pathological
MTX followed by dilatation and curettage, or UAE followed by dilatation examination to confirm the preoperative ultrasonography diagnosis.
and curettage. Data from patients with CSP-II were included in the Data were collected from patients' medical records and operation
present study if they had been treated through direct excision of the notes. Treatment protocols and post-operation data up to the normali-
CSP lesion using laparotomy or if they received UAE treatment followed zation of serum β-hCG levels were retrieved for each patient. Patients
by CSP lesion excision by laparotomy. The present study was approved were contact by telephone and information was collected on the time
by the Institutional Review Board of Xi'an Jiaotong University; obtaining taken after treatment to resume menstruation, on any anomalous
informed consent from patients for the use of medical record data was symptoms experienced, and of any subsequent pregnancies.
waived owing to the retrospective nature of the study and all patients Statistical analyses were performed using SPSS version 20.0 (IBM,
provided verbal consent to participate in telephone interviews. Armonk, NY, USA). Clinical data, including age, gravidity and parity,
Patients who underwent treatment for CSP-I with MTX received an the time interval between the previous cesarean delivery and the
intramuscular MTX injection (50 mg/m2; Shanxi Powerdone diagnosis of CSP, the duration of follow-up after treatment for CSP,
Pharmaceutics Co Ltd., Datong, China). Patients were then evaluated intraoperative blood loss, and the length of hospital stay during
after 1 week; if a patient's serum β-hCG level had decreased by at treatment, were expressed as the mean ± SD or as the median and
least 50%, or to below 2000 mIU/mL, follow-up ultrasonography interquartile range. The Mann–Whitney U test was used to compare
examinations were performed to evaluate chorionic sac volume and the differences between patients receiving different treatments and
vascularization. If initial MTX treatment was ineffective, patients re- P b 0.05 was considered statistically significant.
ceived a further dose and follow-up period. If follow-up ultrasonogra-
phy revealed no growth in CSP masses, dilatation and curettage was 3. Results
performed with abdominal ultrasonography monitoring.
When UAE was included in the treatment of patients who had CSP-I, During the 6-year study period, the CSP to normal pregnancy ratio at
the uterine artery was selectively catheterized using a Rosch hepatic the study institution was 57:16,391. Of these 57 patients, 25 (44%) were
catheter (Terumo Corporation, Tokyo, Japan) and was embolized using classified as CSP-I and 32 (56%) were classified 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 29-
year-old woman with cesarean scar pregnancy type II; the gestational sac had implanted into a previous cesarean scar defect with growth that has infiltrated into the uterine myometrium
and bulges from the uterine serosal surface.
204 Y. Li et al. / International Journal of Gynecology and Obstetrics 134 (2016) 202–207

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

Characteristic CSP-I (n = 24) CSP-II (n = 28) P valueb

Age, y 31.0 (29.0–35.0) 30.5 (27.3–35.0) 0.467

Duration of gestation at diagnosis, d 51 (41.3–62.8) 59.5 (52.3–80.5) 0.017
Gravidity 3 (2–4) 3 (3–4) 0.209
Parity 1 (1–1) 1 (1–1)
Time between previous cesarean delivery and index pregnancy, y 4.1 ± 2.3 7.0 ± 6.3 0.571
Pretreatment serum β-hCG, mIU/mL 5458.5 (2277.3–23,259.8) 3641.0 (1029.8–11,404.5)

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

range of patients diagnosed with CSP was 23–47 years. The duration of study. Among patients with CSP-II, four patients who underwent
pregnancy at the time of CSP diagnosis was 31–112 days. The time CSP lesion excision experienced massive vaginal bleeding
interval between patients' previous caesarean section and the current (N1200 mL); these patients received blood transfusions and
CSP ranged from 0.5 years to 23.0 years. Among the 57 patients underwent emergency ligation of the internal iliac artery. However,
experiencing CSP, 53 (93%) had experienced one previous cesarean this treatment did not resolve the complications and life-saving
delivery, and 4 (7%) had undergone two. Placenta previa during most emergency subtotal hysterectomies were performed for all four pa-
recent pregnancy was reported by one patient. The range of serum tients, resulting in their exclusion from the present study. This re-
β-hCG levels recorded among patients was 13.68–93,207.00 mIU/ sulted in 52 patients being included in the present retrospective
mL. The range of the largest diameter of CSP masses, measured study and telephone interviews. The baseline clinical characteristics
using ultrasonography, was 1.0–7.5 cm in patients with CSP-I and of the patients included in the study are presented in Table 1.
1.0–7.8 cm in patients with CSP-II. Among the potentially eligible Among the patients with CSP-I included in the present study, 14 were
patients with CSP-I, one patient had been referred to the emergency treated with intramuscular MTX injections. The first injection of MTX was
department of the study institution with a vaginal-bleeding not effective in one patient. This individual was managed by administer-
emergency. This patient had been treated with MTX but had ing intramuscular MTX (50 mg/m2) again 8 days after initial MTX admin-
experienced a steady increase in serum β-hCG levels and an increase istration. On day 15, the patient's serum β-hCG level was below
in CSP-mass volume that was visible under ultrasonography 2000 mIU/mL and they underwent ultrasonography examination. Ultra-
examination; the patient underwent CSP lesion excision by sonography examinations revealed no growth in all 14 patients, and
laparotomy and, consequently, was excluded from the present 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) 202–207 205

observed. No UAE-associated adverse effects, including post-

embolization syndrome and pelvic tissue damage, were observed dur-
ing hospitalization. Mild lower abdominal pain continuing for several
days was recorded in all patients who underwent UAE; this pain was
controlled successfully with intravenous flurbiprofen 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
β-hCG levels steadily decreased without the need for additional
treatment in all patients. Following treatment, the time to normaliza-
tion of serum β-hCG levels was 2–6 weeks and 2–5 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 4–8 weeks of treatment (Table 2, Table 3).
From the telephone interviews conducted, 35 patients reported
using contraception after treatment (22 patients reported using intra-
uterine 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

The present study examined the treatment outcomes for 52 patients

with CSP over a 6-year period. Classification using ultrasonography
provided the basis for the management of patients. Including UAE in
Fig. 3. Cesarean scar lesion tissues from a patient with cesarean scar pregnancy type II were the treatment of patients with CSP-I resulted in lower levels of
subjected to pathological examination, confirming the preoperative ultrasonography intraoperative blood loss, reduced hospitalization for treatment, and a
diagnosis. The arrows indicate the chorionic villi.
reduction in the time taken for serum β-hCG levels to normalize com-
pared 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
was performed. UAE before dilatation and curettage was performed in intraoperative blood loss.
the treatment of 10 patients with CSP-I; digital subtraction angiography The accuracy of ultrasonography and magnetic resonance imaging in
images were obtained from patients during embolization (Fig. 2). diagnosing CSP has been demonstrated previously [5,18,19]. It notable
Direct excision of CSP lesions via laparotomy was used to treat 14 that magnetic resonance imaging is a costly diagnostic technique and
patients with CSP-II and UAE was included in the treatment of 14 that this must often be taken into account in clinical environments.
patients with CSP-II before direct excision of CSP lesions. Tissue The use of ultrasonography in diagnosing CSP has the advantages of
samples from CSP lesions were obtained from patients with CSP-II for being non-invasive, simple, and cheap. The level of diagnostic accuracy
pathological examination (Fig. 3). in the present study can be attributed to a combination of transvaginal
No significant difference was found when comparing the time before ultrasonography, a long duration of gestation at the time of diagnosis,
resuming menstruation between the two treatment protocols for and detailed patient histories. The pathological evaluations performed
patients with CSP-I (Table 2). However, the intraoperative blood loss in patients with CSP-II in the study confirmed the accuracy of using
(P b 0.001), length of hospital stay (P = 0.002), and time before normal- ultrasonography for diagnosis.
ization of serum β-hCG levels (P = 0.026) were significantly higher in pa- Considering the severe maternal morbidity that can result from CSP,
tients treated with MTX prior to dilatation and curettage in comparison including massive hemorrhages, uterine rupture, and the occurrence of
with patients treated with UAE before dilatation and curettage (Table 2). an adherent placenta, the induced abortion of a pregnancy following a
No significant difference was recorded in the time before resuming CSP diagnosis is widely accepted [20–22]. However, a previous review
menstruation, the time before serum β-hCG normalization, and the of 751 patients with CSP demonstrated that complications, including
duration of hospitalization between patients with CSP-II treated with hysterectomies, laparotomies, and emergency UAE procedures,
CSP lesion excision alone and those treated with UAE before lesion occurred in 331 (44.1%) patients [19]. The aim of classifying CSP prior
excision. Intraoperative blood loss was lower in patients who underwent to treatment in the present study was to minimize the risk of severe
UAE prior to CSP lesion excision (P b 0.001) (Table 3). complications based on the features of different CSP types. In patients
During treatment and follow-up, no MTX-related adverse events, with CSP-I, the intention behind the choice of treatment was to avoid
including leukopenia, alopecia, and abnormal liver function, were 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 Patients treated with uterine artery embolization before dilatation P valueb
and curettage (n = 14) and curettage (n = 10)

Duration of hospitalization, d 8.5 (8.0–14.3) 5.5 (4.0–7.5) 0.002

Time before β-hCG normalization, wk 3.5 (2.0–4.0) 2.0 (1.0–3.0) 0.026
Intraoperative blood loss, mL 200.0 (172.5–257.5) 55.0 (30.0–72.5) b0.001
Time before resuming menstruation, d 31.0 (29.0–39.3) 30.5 (29.8–32.3) 0.625

Abbreviations: CSP-I, cesarean scar pregnancy type I; β-hCG, beta human chorionic gonadotropin.
Values are given as median (interquartile range) unless indicated otherwise.
Mann–Whitney U test.
206 Y. Li et al. / International Journal of Gynecology and Obstetrics 134 (2016) 202–207

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

Variable Patients treated with direct excision of CSP lesion Patients treated with uterine artery embolization direct excision of CSP P valueb
(n = 14) lesion (n = 14)

Duration of hospitalization, d 9.0 (7.8–10.3) 8.0 (6.0–9.0) 0.150

Time before β-hCG normalization, wk 2.0 (1.0–3.3) 2.0 (1.0–2.0) 0.114
Intraoperative blood loss, mL 575.0 (450.0–612.5) 265.0 (200.0–300.0) b0.001
Time before resuming menstruation, d 34.5 (32.0–36.3) 34.5 (31.3–37.5) 0.769

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

treatment failures. For patients with CSP-II, the preservation of patient individualizing patient treatment. Combining UAE with dilatation and
fertility and a reduction in the risk of massive hemorrhage were priori- curettage in the treatment of patients with CSP-I patients, and with
ties. Individualizing treatment according to the different CSP subtypes CSP-lesion excision in the treatment of patients with CSP-II are effective
resulted insubstantial improvements in clinical outcomes. treatment options for these CSP subtypes. However, long-term follow-
Systemic MTX injections, dilatation and curettage, and UAE are up and further research are still warranted.
treatments that have all demonstrated high complication rates previ-
ously [19]. Consequently, combining therapeutic approaches should be
considered when selecting the treatment options. Combining MTX ther- Conflicts of interest
apy with suction curettage in the treatment of CSP has been reported to
result in a shorter resolution time for CSP masses and serum β-hCG The authors have no conflicts of interest.
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 References
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