A combination of laparoscopy and bilateral uterine artery occlusion for the treatment of type II cesarean scar pregnancy: a retrospective analysis

Abstract

Objective

We investigated the efficacy of a combination of laparoscopy and bilateral uterine artery occlusion (BUAO) for the treatment of type II cesarean scar pregnancy (CSP).

Methods

Patients with type II CSP underwent laparoscopy + bilateral uterine artery embolization (control group) or laparoscopy + BUAO (study group). Data regarding the duration of surgery, intraoperative hemorrhage, postoperative complications, the duration of the hospital stay, and the costs of hospitalization were retrospectively collected. One year later, the time to the return of the β-human chorionic gonadotropin (β-hCG) concentration to normal and to the return of menstruation were compared.

Results

The duration of surgery, time to the return of menstruation, and incidence of postoperative complications in the study group were significantly less than in the control group, but there was no significant difference in the time for β-hCG to return to normal or the volume of intraoperative hemorrhage. The duration of hospitalization and costs for the control group were higher than those for the study group.

Conclusion

Laparoscopy in combination with BUAO is associated with minimal trauma, rapid recovery, a short duration of surgery, low cost of hospitalization, and a low postoperative complication rate. Thus, it represents a useful new surgical treatment for type II CSP.

Keywords

Type II cesarean scar pregnancy laparoscopy bilateral uterine artery embolization bilateral uterine artery occlusion intraoperative hemorrhage postoperative complication menstruation duration of surgery hospitalization

Introduction

Cesarean scar pregnancy (CSP) is a specific type of ectopic pregnancy (EP) in which the fertilized egg is deposited in the uterine incisional scar of a woman who previously underwent cesarean delivery. Symptoms usually develop during early pregnancy (up to 12 weeks’ gestation), and this condition is therefore a late complication of cesarean delivery.¹ The incidence of CSP has been reported to be 1 in 2216 to 1 in 1800, it occurs in 1.15% of women who have a history of cesarean delivery, and accounts for 6.1% of EPs in women with a history of cesarean delivery.² However, over the past 10 years, the incidence of CSP has increased rapidly, owing to the increase in the number of cesarean sections being performed worldwide, and especially in mainland China, with the introduction of the two-child policy.³

CSP can be categorized as type I (endogenic), characterized by growth toward the uterine cavity, and type II (exogenic), characterized by deep invasion of the uterine defect across the uterine serosa and toward the bladder and abdominal cavity.⁴ If it is not diagnosed and treated early, type II CSP can result in uncontrollable hemorrhage, uterine rupture, damage to surrounding organs, and hysterectomy, which have negative effects on the reproductive health and lives of women.⁵ The principal treatment options for type II CSP are uterine curettage, hysteroscopy evacuation, and laparotomy or laparoscopy to excise the gestational sac from the cesarean scar. Several approaches have been developed to limit the blood loss that occurs during the management of CSP, including uterine artery embolization (UAE), intramyometrial injection of vasoconstrictors, and the placement of a Foley balloon catheter.^6–10 However, to date, no consensus has been reached regarding the best treatment method.

After type II CSP has been diagnosed, most clinicians believe that a combination of laparoscopy and BUAE represents the best choice for surgical treatment.¹¹ However, this may be associated with the risks of radiation injury, procedure-related complications, and adverse effects, such as over-embolization, incomplete embolization, and failed embolization. In addition, it is an expensive procedure. Therefore, in the present study, we aimed to compare the efficacy of laparoscopy in combination with bilateral UAE (BUAE) or bilateral uterine artery occlusion (BUAO) for the treatment of patients with type II CSP to improve knowledge regarding the optimal treatment of patients with type II CSP.

Methods

Participants

The clinical data for the patients who experienced CSP between January 2015 and December 2021 were analyzed retrospectively. During this process, all the information that could identify the patients was deleted. According to the surgical procedure used, the participants were allocated to a control group (laparoscopy + BUAE) and study group (laparoscopy + BUAO).

The inclusion criteria were (1) a history of cesarean delivery, (2) a diagnosis of CSP that was based on clinical symptoms and imaging findings, and (3) a lack of treatment prior to admission. The exclusion criteria were (1) severe disease, including cardiac, hepatic or renal disease; (2) inability to diagnose type II CPS, (3) a history of pelvic surgery for other reasons or a history of other uterine diseases; (4) a coagulation disorder, (5) a lack of suitability for surgery, (6) a psychiatric disorder, and (7) poor compliance.

Criteria for diagnoses of CSP and type II CSP

CSP was diagnosed when transvaginal ultrasonographic examination showed that (1) the uterine cavity and cervical canal were empty (there was no gestational sac within); (2) the gestational sac had implanted near the scar or niche relating to the previous uterine incision, usually with fetal buds or a fetal heartbeat apparent; (3) there was disruption of the continuity of the myometrium of the anterior wall of the uterus, with marked thinning or loss of the myometrium between the gestational sac and the bladder; and (4) there was abundant blood flow around the gestational sac (identified using Doppler-flow imaging).¹²

Type II CSP was diagnosed when (1) the gestational sac was completely embedded in the myometrium of the uterine scar and bulged out towards the bladder; (2) the uterine cavity and cervical canal were empty; and (3) there was significant thinning or absence of the myometrium between the gestational sac and bladder⁴ (Figure 1a).

Figure 1.

Representative images of the participants. (a) Preoperative ultrasonographic image of a participant with type II CSP. (b) Ultrasonographic image of a participant with type II CSP 2 weeks following laparoscopy + BUAO. (c) Intraoperative image of left uterine artery occlusion and (d) intraoperative image of right uterine artery occlusion. CSP, caesarean scar pregnancy; BUAO, bilateral uterine artery occlusion.

The reporting of the study conforms to the STROBE guidelines.¹³

Surgical procedures

BUAE was performed by an experienced and certified team who was highly familiar with the pelvic vascular anatomy, and laparoscopic surgery was performed by the same experienced surgeon. The combination of laparoscopy and BUAE was performed in two stages: BUAE, followed by laparoscopic surgery.

BUAE was performed as follows. After the successful induction of anesthesia by local infiltration, the participant was placed in a supine position, a right femoral artery was punctured, a vascular sheath was inserted, and a hysterosalpingography catheter was fed through the vascular sheath to permit bilateral uterine artery angiography, the measurement of the size and extent of the lesion, and assessment of the blood flow. Methotrexate 100 mg and 1- to 3-mm gelatin sponge pellets were then sequentially injected into both uterine arteries under angiographic monitoring. After re-angiography to confirm successful embolization, the catheter and vascular sheath were removed. The puncture site was then compressed for 20 minutes and a pressure bandage was applied. The right lower limb of each participant was immobilized for 12 hours and the skin temperature difference and dorsalis pedis artery pulsations were closely monitored. Twenty-four hours following BUAE, if the patient was free of complications, laparoscopic surgery was performed.

Laparoscopic surgery was performed as follows. After the induction of general anesthesia, the participant was placed in a supine position with their hips elevated at approximately 30°, pneumoperitoneum was established, and the intraabdominal pressure was maintained at 13 mmHg. Next, under laparoscopic guidance, an ultrasonic knife was used to break down the adhesion and expose the lower segment of the uterus. Typically, the site where the anterior wall of the lower segment of the uterus and the bladder peritoneum were folded was swollen, protruded outwards, and was a purple-blue color. A solution of posterior pituitary hormone (12 U of posterior pituitary hormone in 60 mL of saline) was then injected into the lower uterine segment and the interstitial space between the bladder and cervix. The vesico–uterine peritoneal reflection was incised and the bladder was displaced downward, then the ultrasound knife was used to make a transverse incision at the site of the pregnancy. The pregnancy tissue was then excised, the scar tissue was trimmed, the mucosa was sutured using a 1-gauge purse suture, the myometrium and serosa were sutured, the vesico–uterine peritoneal reflection was closed, and the pelvic cavity was flushed with saline. At that time, the absence of ongoing hemorrhage was confirmed and the procedure was completed.

The combination of laparoscopy and BUAO was performed as follows. Following the induction of general anesthesia, the patient was placed in a supine position with their hips elevated at approximately 30°, pneumoperitoneum was established, and the intraabdominal pressure was maintained at 13 mmHg. The laparoscope and other instruments were then inserted, and the uterus, bilateral adnexa, and pelvis were explored. The broad ligament was incised 2 cm above the sacral ligament, the ureter was located according to the MR 3D reconstruction, and the main trunk of the uterine artery was freed above the ureter. A 0-1 absorbable wire was then passed through the base of the uterine artery, a slipknot was tied to temporarily occlude flow through the uterine artery, and the opposite side was treated in the same way (Figure 1c, d). Subsequently, the procedure was the same as the laparoscopic procedure performed for the control group. After flushing of the pelvic cavity, the ligatures were removed from the uterine arteries, taking care not to cause vessel rupture. The anesthetist was then asked to increase the blood pressure of the participant into the normal range, and the procedure was completed after 5 minutes of observation to ensure no hemorrhage was occurring.

Following the procedures, a double-lumen Foley balloon catheter was placed in the isthmus of the participants in both groups and 15 to 20 mL of saline was injected to compress the uterine wound and provide drainage. All the procedures were performed by the same team of surgeons. The criteria for discharge were as follows: (1) no postoperative bloody vaginal discharge, (2) a postoperative β-HCG concentration of 1000 to 2000 mUnits/mL, and (3) appropriate healing of the abdominal surgical wound.

Postoperative monitoring

The duration of surgery, the quantity of intraoperative hemorrhage, the presence or absence of postoperative complications, the duration of the hospital stay, and the costs of hospitalization were recorded. All the participants were followed up through outpatient appointments and telephone contact during the year following their procedures. Their β-hCG concentration was measured once weekly postoperatively until it returned to normal, and the time at which this happened, and the time at which menstruation returned, were recorded. Transvaginal ultrasonography was performed during the third postoperative month, during the ovulation phase of the menstrual cycle of each participant, to measure the thickness of the muscle layer of the anterior wall of the lower uterine segment.

Statistical analysis

Data were analyzed using SPSS version 22.0 (IBM Corp., Armonk, New York, USA). Continuous data are expressed as mean ± standard deviation and the groups were compared using the independent samples t-test. Categorical data are expressed as number (percentage) and the groups were compared using the chi-square test. P < 0.05 was regarded as indicating statistical significance.

Ethics approval and consent to participate

This study was approved by the Medical Ethics Committee of the First Affiliated Hospital of Xi’an Medical University (approval no. XYYFY2023LSK-032). The necessity for informed consent was waived by the committee because of the retrospective nature of the study.

Results

Following the application of the inclusion and exclusion criteria, 88 of the total of 561 patients remained for enrollment in the study. The control group comprised 45 participants, who were aged 26 to 37 years (mean age 31.56 ± 2.22 years), had undergone between two and five pregnancies (mean 2.71 ± 0.84 pregnancies), were diagnosed at gestational week 3.5 to 11.7 (mean 7.75 ± 1.87 weeks), had a gestational sac diameter of 2.13 to 5.18 cm (mean 3.42 ± 0.82 cm), and had a mean preoperative β-human chorionic gonadotropin (β-hCG) concentration of 26,017 ± 4,769 mUnits/mL. The control group comprised 43 participants who were 28 to 36 years old (mean age 32.19 ± 1.53 years), had undergone two to four pregnancies (mean 2.95 ± 0.69 pregnancies), were diagnosed at gestational week 4.5 to 11.2 (mean 7.76 ± 1.60 weeks), had a gestational sac diameter of 2.03 to 4.86 cm (mean 3.43 ± 0.75 cm), and a mean preoperative β-hCG of 25,071 ± 4430 mUnits/mL. Eighty-one of the fetuses had cardiac activity, of which 40 were in the study group and 41 in the control group. The myometrial thickness of the anterior uterine wall of the entire cohort was <3 mm (range, 1.0 to 2.9 mm, median 2.1 ± 0.3 mm), according to measurements made using magnetic resonance (MR) or ultrasonographic images. There were no significant differences in the age, parity, week of gestation, β-hCG concentration prior to surgery, or diameter of the gestational sac between the two groups (Table 1).

Table 1.

Comparison of the general clinical data of the two groups.

	Study group (n = 43)	Control group (n = 45)	P
Age (years)	32.19 ± 1.53	31.56 ± 2.22	0.126
Duration of gestation (weeks)	7.76 ±1.60	7.75 ± 1.87	0.975
Parity (n)	2.95 ± 0.69	2.71 ± 0.84	0.144
Gestational sac diameter (cm)	3.43 ± 0.75	3.42 ± 0.82	0.959
Presence of fetal heart activity (n)	40	41	0.977
Preoperative myometrial thickness (mm)	2.19 ± 0.29	2.09 ± 0.32	0.160
Preoperative β-hCG (mUnits/mL)	25,071 ± 4,430	26,017 ± 4,769	0.338
Duration of the procedure (min)	70.70 ± 15.31	105.29 ± 12.67	<0.001

β-hCG: β-human chorionic gonadotropin. Data are mean ± SD or n. The groups were compared using the independent samples t-test or chi square test, as appropriate.

The procedures were completed successfully in all the participants in both groups. There was no significant difference in the volume of intraoperative bleeding between the two groups. The control group underwent longer procedures (control group: laparoscopic surgery and BUAE; study group: laparoscopic surgery and BUAO) (P < 0.001), had a higher incidence of postoperative complications (P = 0.002), had longer hospital stays (P < 0.001), and had higher hospitalization costs (P < 0.001) than the study group (Tables 1, 2, and 3).

Table 2.

Comparison of the intraoperative and postoperative data for the two groups.

	Study group (n = 43)	Control group (n = 45)	P
Intraoperative hemorrhage (mL)	40.44 ± 2.12	42.11 ± 5.60	0.070
Hospital stay (days)	5.51 ± 0.51	7.40 ± 1.16	<0.001
Cost of hospitalization (yuan)	15,353 ± 1,816	22,440 ± 1,064	<0.001
Time taken for β-hCG to return to normal (days)	28.09 ± 0.92	28.53 ± 1.12	0.084
Time taken for menstruation to return (days)	42.00 ± 4.93	49.00 ± 4.69	<0.001
Endometrial thickness 3 months following surgery (mm)	9.11 ± 1.32	8.75 ± 1.66	0.267

β-hCG: β-human chorionic gonadotropin. Data are mean ± SD, and the groups were compared using the independent samples t-test.

Table 3.

Comparison of the incidence of post-operative complications in the two groups.

	Study group (n (%))	Control group (n (%))	χ²	P
Fever	1 (2.33)	3 (6.67)	9.831	0.002
Nausea and vomiting	0 (0)	2 (4.44)
Abdominal pain	2 (4.65)	5 (11.11)
High liver enzyme activities	0 (0)	2 (4.44)
Endometrial atrophy	0 (0)	2 (4.44)
Low menstrual flow	1 (2.33)	3 (6.67)

With respect to recovery, the time taken for the β-hCG concentrations of the participants to return to normal was similar in the two groups (28.09 ± 0.92 days for the control group and 28.53 ± 1.12 days for the study group). However, the time taken for menstruation to return was longer in the control group than in the study group (49.00 ± 4.69 days vs. 42.00 ± 4.93 days, respectively; P < 0.001) (Table 2). During the third postoperative month, a transvaginal ultrasonographic examination was performed during the ovulatory phase of the menstrual cycle of each participant to measure the thickness of the muscle layer of the anterior wall of the lower segment of the uterus, and we found that the thicknesses were similar in the two groups (9.11 ± 1.32 mm for the control group and 8.75 ± 1.66 mm for the study group) (Figure 1b).

During the 1-year follow-up period, six participants became pregnant again in the control group and three in the study group. Of these nine, five delivered a baby successfully, two terminated their pregnancy, and two had recurrent CSP and underwent surgical treatment.

Discussion

Cesarean scar pregnancy, although an extremely rare form of EP, is a subject of increasing interest for clinicians, and its incidence and frequency of diagnosis have been increasing.^11,14 The serious life-threatening complications of CSP include both maternal and fetal morbidity and mortality.⁵ Medical treatment or the use of medication in combination with dilatation and curettage can achieve satisfactory results in some patients,^15,16 but surgery remains the most effective treatment.¹⁷ In type II CSP, the fertilized egg implants in the deep muscle layer of the uterine scar and the gestational sac grows towards the abdominal cavity and bladder, with serious consequences including hemorrhage and uterine rupture early in pregnancy, owing to the thin epithelium of the uterus wall.¹⁸ Diakosavvas et al.¹⁹ has suggested that hysteroscopic resection can be used for the treatment of CSP types I and II, but owing to the deeper location of the pregnancy in the defect in type II CSP and its growth towards the surface of the uterine serosa, beneath the bladder, hysteroscopy may be associated with a high risk of uterine perforation and bladder injury. Therefore, we prefer laparoscopic surgical treatment.

The use of laparoscopic surgery permits full exposure of the surgical field, exploration of the pelvic and abdominal cavities, the bladder to be freed and displaced downward, thereby minimizing the risk of bladder injury, and the removal of the pregnancy tissue and scar tissue infiltrated by the pregnancy. It also permits surgeons to reinforce and reconstruct the lower uterine segment and to restore its normal anatomy, thereby reducing the incidence of recurrent CSP and the risk of uterine rupture.^20,21 BUAE is an effective means of controlling hemorrhage, not only by preventing blood reaching the placental tissue implanted in the scar, causing its necrosis and resorption, but also by reducing intraoperative hemorrhage, reducing the length of the procedure, and improving its success rate. The gelatin sponge used for BUAE dissolves and is absorbed within 2 to 3 weeks, and the uterine blood flow is completely restored to normal, which preserves the patient’s reproductive function.^22,23 Therefore, a combination of laparoscopy and BUAE is an effective surgical treatment of Type II CSP, and allows excellent visualization of the pelvis and pregnancy mass, complete removal of the pregnancy mass, and the repair of the uterus. It also reduces hemorrhage, shortens the procedure, and reduces the risk of complications. However, the widespread use of laparoscopy in combination with BUAE for the treatment of CSP has not been associated with a reduction in the incidence of postoperative complications,²⁴ such as lower abdominal pain, post-embolization syndrome, fever, allergic reaction, incomplete embolization, or over-embolization. Shamy et al.²⁵ found that up to 8% of women develop permanent ovarian failure following UAE. In addition, Tropeano et al.²⁶ reported a case of amenorrhea following UAE in a 44-year-old woman that was confirmed by hysteroscopy and histology to be the result of endometrial atrophy and an impairment in endometrial proliferation following the procedure. Chrisman et al.²⁷ assessed the menstruation and fertility of 66 patients following UAE, and found that 10 had abnormal menstruation, 9 of whom received diagnoses of ovarian failure. In addition, the incidence of intrauterine adhesions following UAE has been shown to be 10.2% to 14%,^26,28 and these lesions seriously affect the fertility of the patients. Qiu et al.²⁹ reported the case of a patient with CSP who developed acute pulmonary embolism following UAE, and although the incidence of pulmonary embolism following UAE is extremely low, it is associated with a high risk of mortality. Fever, abdominal pain, and high circulating liver enzyme activities were also identified in the patients who underwent BUAE in the present study. Three months following the surgery, an endometrial examination during the ovulatory phase of the menstrual cycle revealed significant endometrial thinning and poor blood flow in two patients following BUAE. The explanation for this was likely the difficulty in restoring normal uterine blood flow during the early stages of collateral circulation following BUAE, which affects endometrial growth.

To reduce the risk of complications associated with UAE, superior surgical procedures are required. Wang et al.³⁰ treated six clinically stable patients with CSP using vacuum aspiration following laparoscopic uterine artery ligation, and found that laparoscopic temporary BUAO using silicone tubing is an effective, minimally invasive means of reducing blood loss during vacuum aspiration in patients with CSP. In addition, Lata et al.³¹ performed laparoscopic resection of cesarean scar-associated EPs and repair in five patients with CPS by temporarily occluding both uterine arteries, resulting in a reduction in intraoperative hemorrhage and satisfactory surgical results. Alzamora et al.³² reported a case of a patient with CPS who had failed to respond to pharmacologic treatment, but was successfully treated by laparoscopy in combination with vascular clamp placement, and concluded that intraoperative occlusion of both uterine arteries reduces hemorrhage. Kathopoulis et al.³³ used metal clips to temporarily occlude both uterine arteries during laparoscopic surgery in two patients with CSP, which reduced the blood supply to the niche and permitted the successful extraction of pregnancy products, scar removal, and repair of the deficit. Both Qian et al.³⁴ and Lina et al.¹⁸ also concluded that the intraoperative temporary occlusion of both uterine arteries reduces intraoperative hemorrhage, and the present findings are consistent with this conclusion.

Compared with BUAE, BUAO is associated with a smaller amount of intraoperative hemorrhage, and when used in combination with laparoscopy, also permits the removal of CSP tissue and the repair of the uterus. In the present study, the study group underwent significantly shorter procedures, principally because the BUAE procedure used in the control group was longer than the time taken for the intraoperative separation and occlusion of the uterine arteries in the study group. The time taken for menstruation to return was shorter and the incidence of complications was lower in the study group than in the control group. We propose that there are two main reasons for this: (i) the complications associated with BUAE are unavoidable, and (ii) it takes longer for the blood supply to return to normal following embolization. Although the collateral circulation can compensate for the loss of uterine artery patency, the uterus remains ischemic following the latter procedure, which not only predisposes toward complications, but also delays its recovery. In contrast, in the study group, following the removal of the CSP tissue and uterine repair, the blood flow through both uterine arteries was immediately reinstated, facilitating uterine recovery. Therefore, we believe that the use of laparoscopy in combination with BUAO avoids the disadvantages associated with BUAE, making it an ideal treatment option for Type II CSP. However, this requires the physician to have extensive clinical experience of laparoscopy and to be skilled in minimizing the intraoperative risks.

The present study had some limitations. First, it was a retrospective analysis, and the parameters assessed were not comprehensive and may have involved bias. Thus, more comprehensive data collection and further analysis of these techniques are needed. Second, the sample size was small. Third, the use of laparoscopy in combination with BUAO and BUAE were evaluated retrospectively using clinical records, with a postoperative follow-up period of only 1 year. Therefore, in the future, more comprehensive, prospective, large-scale studies should be performed.

Laparoscopy in combination with BUAO or BUAE for the treatment of type II CSP has the advantages of minimal trauma, a high level of efficacy, and a rapid recovery, and in particular, a low incidence of hemorrhage and a high incidence of resolution of type II CPS. However, compared with BUAE, laparoscopy in combination with BUAO has the advantages of being a shorter procedure, and being associated with a lower cost of hospitalization and a lower incidence of postoperative complications. Therefore, it represents a new and effective surgical method for the treatment of type II CSP.

Footnotes

Acknowledgements

The authors thank the nurses of The First Affiliated Hospital of Xi’an Medical University for their advice and cooperation.

Author contributions

FX: Identification of the research topic; Confirmation of the results of the statistical analysis HW: Data collection; Revision of the manuscript. WW: Writing of the manuscript. The authors all read and approved the final version of the manuscript.

Declaration of conflicting interest

The authors declare that there is no conflict of interest.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

ORCID iD

Fangfang Xue

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