Temporary bilateral uterine artery occlusion in the control of hemorrhage: A case report and review of literature

Abstract

BACKGROUND

Intramural pregnancy is rare, with an unclear etiology and pathophysiology. Surgical, medical, and expectant management options are available for this condition. However, most reported cases are managed surgically. Despite the risks of massive intraoperative bleeding and acute and long-term complications, uterine artery embolization is often selected. Temporary occlusion of the bilateral uterine arteries during surgery is associated with fewer complications.

CASE SUMMARY

We reported the case of a patient who was diagnosed with intramural pregnancy approximately one month after medical abortion. We performed laparoscopic resection with hysteroscopy. Since the lesion had abundant blood flow, we temporarily blocked the bilateral uterine arteries to prevent massive intraoperative bleeding. The surgical process went smoothly. The postoperative course was uneventful.

CONCLUSION

Temporary occlusion of the bilateral uterine arteries in the treatment of intramural pregnancy may prevent excessive uterine bleeding during surgery.

Key Words: Intramural pregnancy; Hysteroscopy; Laparoscopic surgery; Uterine artery temporary occlusion; Case report

Core Tip: Intramural pregnancy is rare. There are few reports on temporary uterine artery occlusion for the treatment of intramural pregnancy. Here, we review studies on intramural pregnancy and report bilateral uterine artery occlusion during laparoscopic surgery and hysteroscopy for intramural pregnancy. The surgical process and postoperative course were uneventful.

INTRODUCTION

Intramural pregnancy is rare and represents less than 1% of all ectopic pregnancies[1,2]. Intramural pregnancy is characterized by the presence of the gestational sac in the uterine myometrium without any connection to the uterine cavity[3]. In intramural pregnancy, uterine rupture is potentially fatal, as it can lead to severe hemorrhage and hysterectomy. Early diagnosis of intramural pregnancy is very important. Surgical, including uterine artery embolization (UAE), medical, and expectant management options are available for this condition, and the optimal method depends on the size and location of the gestational sac, gestational age, and the patient's desire for future fertility. Here, we report laparoscopic surgery and hysteroscopy for intramural pregnancy after medical abortion. The bilateral uterine arteries were temporarily blocked during surgery.

CASE PRESENTATION

Chief complaints

A 41-year-old patient, gravidity 3, parity 1, artificial abortion 2, was admitted to the hospital because of a small amount of vaginal bleeding for approximately half a month after medical abortion.

History of present illness

The patient underwent medical abortion on December 13, 2021. The gestational sac was successfully discharged. After medical abortion, a small amount of vaginal bleeding persisted for one week. Approximately one month later, on January 27, 2022, the patient experienced vaginal bleeding again, which initially appeared to be a normal amount of menstruation. Afterward, a small amount of intermittent vaginal bleeding persisted.

History of past illness

She was healthy without internal medical disease and had no history of surgery.

Personal and family history

She denied any family history of inherited disease or malignant tumors.

Physical examination

Physical examination revealed a normal sized uterus with no tenderness and no abnormalities in the uterine cervix or abdomen. There was a small amount of vaginal bleeding.

Laboratory examinations

On February 9, 2022, her serum β-human chorionic gonadotropin (β-hCG) level was 2649.00 mIU/mL.

Imaging examinations

Three-dimensional transvaginal examination revealed an abnormal echo approximately 1.0 cm × 0.5 cm × 0.4 cm in size in the uterus cavity near the left uterine corner, and the echo extended to the myometrium of the uterus fundus. Color Doppler ultrasound revealed abundant blood flow around it (the “ring of fire” “sign”; Figure 1). Doppler ultrasound also revealed highly vascular tissue approximately 1.7 cm × 1.6 cm × 1.3 cm in size in the left bottom muscle layer, with detectable arterial and venous abnormalities, low resistance and high-speed blood flow, suggesting an arteriovenous fistula. T1 and T2 images on pelvic magnetic resonance imaging revealed a nodule approximately 1.5 cm in diameter with equal shadows and signals within the myometrium in the left wall of the uterus and no significant limitation in diffusion.

Figure 1 Imaging examinations. A: Color Doppler ultrasound image showing abundant blood flow around it (the "ring of fire" sign); B: Pelvic magnetic resonance imaging showed a nodular measuring approximately 1.5 cm within the myometrium in the left wall of the uterus.

MULTIDISCIPLINARY EXPERT CONSULTATION

The diagnosis was unsure, maybe intrauterine residue, cornual pregnancy, gestational trophoblastic disease or intramural pregnancy.

FINAL DIAGNOSIS

Intramural pregnancy was diagnosed via surgical and pathological examinations.

TREATMENT

We performed hysteroscopy under general anesthesia, and although no apparent pregnant tissue was found, a membrane-like substance was observed in the uterine cavity near the left uterine horn and tubal ostia. We performed uterine curettage and scraped out a small amount of endometrial tissue.

We subsequently performed laparoscopic surgery and found no apparent adhesion or blood in the pelvic cavity. The uterus was average in size and positioned posterior, with no obvious myoma on the surface or protrusions in the bilateral uterine horns. We considered the possibility of intraoperative hemorrhage and decided to temporarily block the bilateral uterine arteries with titanium clamps. This step was essential. First, we exposed the uterine arteries by separating the anterior leaf of the broad ligament, dissecting the internal iliac artery and locating the uterine artery originating from the internal iliac artery. We then used titanium clips to block the bilateral uterine arteries intuitively. On the basis of the preoperative imaging examination, unipolar electrocoagulation was performed to cut the serous membrane layer of the left posterior wall near the uterine corner approximately 2 cm deep, where villous tissue with a diameter of approximately 1 cm was visible (Figure 2). The tissue was removed entirely. An enlarged excision measuring 0.5 cm was made in the myometrium along the outer edge of the villous tissue. Bipolar electrocoagulation was performed to stop the bleeding on the wound surface, and 1/0 absorbable sutures were used to close the uterine wound layer by layer, restoring the typical anatomical structure of the uterus. The titanium clips were removed from the bilateral uterine arteries. The surgical process went smoothly.

Figure 2 Surgical images. A: Hysteroscopy showing no apparent pregnant tissue but rather a membrane-like substance measuring approximately 1 cm × 1 cm near the left uterine horn; B: We cut the serous membrane layer near the left uterine corner approximately 2 cm deep, where villous tissue measuring approximately 1 cm in diameter was visible; C: The uterine artery was occluded with titanium clamps.

OUTCOME AND FOLLOW-UP

The postoperative course was uneventful. The patient was discharged on the 7^th postoperative day. Pathological examination confirmed the diagnosis of intramural pregnancy. The serum β-hCG level was normal one week after surgery. Until July 2024, the patient was healthy. She had no desire to become pregnant again.

DISCUSSION

Intramural pregnancy is rare and represents less than 1% of all ectopic pregnancies[1,2]. Intramural pregnancy is characterized by the presence of the gestational sac in the uterine myometrium without any connection to the uterine cavity[3]. Considering that intramural ectopic pregnancy is not common, there is a lack of information on the clinical features, available treatments, and long-term reproductive outcomes of patients, as most information is conveyed in case reports. We reviewed publications on intramural pregnancy from August 2017 to August 2024 and studied and reviewed 12 articles (Table 1). The cause and pathophysiology of intramural pregnancy are unclear. Adenomyosis, infertility, uterine curettage, cesarean section, myomectomy, and pelvic infection are among the potential reasons[4]. Nearly every prior procedure mentioned in the 12 studies retrieved during the search for relevant literature involved in the uterine cavity[5-16]. One possible risk factor for the case we reported here was the patient's history of medical abortions. However, there are also two cases in which there has not been a uterine cavity operation, pregnancy or any other remarkable history of gynecological diseases[5,6]. Thus, in-depth study of the causes and factors contributing to intramural pregnancy is still necessary.

Table 1 Summary of the findings reported in the studies identified by the literature search.

	Ref.	Reproductive history	Previous uterine surgery	Other medical history	Location of pregnancy	Treatment	Intraoperative blood loss (mL)	Gestational age (week)
1	Guo et al[5], 2023	G3P2	No	Primary dysmenorrhea	Inside the myometrium below the right uterine horn	Hysteroscopy combined with laparoscopy, used pituitrin to help find the gestational sac	Approximately 10	-
2	Aouragh et al[6], 2024	G0P0	No	No	In the right side closely located to the cornua	Laparotomy	-	6
3	Kubo et al[7], 2024	G2P0	Two dilatation and curettage procedures	No	In the anterior muscular layer of the uterus	Total laparoscopic wedge resection using intraoperative ultrasonography	45	6
4	Truong et al[8], 2022	G2P1	Laparoscopic surgery for an ectopic pregnancy	No	In the myometrium layer close to the uterine fundus	Laparotomy, hysterectomy	Under 100	-
5	Xie et al[9], 2022	G1P0	Laparoscopic salpingotomy, laparoscopic bilateral salpingectomy for bilateral tubal pregnancy, hysteroscopy three times	Secondary infertility	In the left side of the anterior uterus	Laparoscopic surgery, with methotrexate injected into the myometrium	-	7
6	Hlinecká et al[10], 2022	G1P0	Cesarean section, hysteroscopic resection of retained products of conception	No	-	Laparoscopic artery occlusion and removal of pregnancy	-	7
7	Song et al[11], 2020	G6P2	Uterine curettage twice	No	In the posterior wall of the uterus	Diagnostic chemotherapy with (Etoposide+Methotrexate+Actinomycin D+cyclophosphamide), but false.	-	-
8	Nees et al[12], 2020	G1P0	Cesarean section	No	Near the left tubal os	Laparotomy with uterine wedge resection	-	-
9	Liu and Wu[13], 2020	G2P1	Ectopic pregnancy, IVF treatment and had 2 implantation failures in the first cycle of IVF.	No	In the right side of the posterior uterine	Exploratory laparoscopy, hysteroscopy and conservative surgical excision	100	7
10	Zhang et al[14], 2019	G1P1	Cesarean section	No	In the posterior wall below the left horn of the uterus	Laparoscopic surgery, with methotrexate injected into the myometrium	-	-
11	Vagg et al[15], 2018	G2P2	Open myomectomy	No	In the right uterine horn	A midline laparotomy, total abdominal hysterectomy, and bilateral salpingectomy	-	12
12	Mahmoud and Mahmoud[16], 2017	G8P7	Cesarean section	No	Anterior myometrium of the lower uterine segment, cesarean scar pregnancy	Exploratory laparotomy	-	8

Researchers believe that intramural pregnancies should be managed individually[17]. Owing to the rarity of intramural pregnancy, there are no established guidelines for treatment at present. Various factors, such as the patient's state, conception location, gestational age, and desire to preserve fertility, influence the treatment selected for intramural pregnancy. A range of management strategies, including methotrexate treatment, laparoscopic surgery, laparotomy surgery, and expectant management, have been attempted. Methotrexate is administered systemically via a local injection and has been used successfully to arrest pregnancy development in cases of intramural pregnancy[18-20]. Katano et al[20] managed intramural pregnancy in the 8^th week of gestation, as evidenced by an hCG level of 4000 IU/L, with laparoscopic and transvaginal local injections of methotrexate and reported that such an approach is an effective way to preserve reproductive potential. Memtsa et al[21] described a case in which the hCG level was 1159 IU/L and was managed with an injection of methotrexate. The hCG test was negative 6 weeks thereafter. The patient experienced transient severe lower abdominal pain. The major disadvantages of medical treatment for ectopic pregnancy are the need for prolonged follow-up and uncertainty about the effects on future fertility and pregnancies[22]. In our case, intramural pregnancy is difficult to diagnose via imaging examination and requires intraoperative and pathological examination for diagnosis; however, the patient refused treatment with methotrexate. Therefore, we adopted conservative surgical management.

Expectant management was occasionally applied in a case report in which the serum β-hCG level was 9.5 mIU/mL[23]. After a literature review, most of the case reports involved conservative surgical management, such as laparoscopic surgery[15], hysteroscopic surgery[24], and UAE [25]. Shen et al[26] reported that 10 of the 17 cases reported were successfully managed with laparoscopic surgery, indicating that laparoscopic surgery was more widely performed than other methods were for treating early intramural pregnancy; moreover, 8/12 cases reported were also treated with laparoscopic surgery. However, it is important to note that patients in mid- or late-term pregnancy should consider a cesarean section as their first option since they may experience excessive bleeding and their uterus may not be able to tolerate laparoscopic surgery. Auer-Schmidt et al[24] successfully managed intramural pregnancy with hysteroscopic surgery using a resectoscope loop to resect the sac through a visualized false tract. However, most of the time, hysteroscopy is used to examine the uterine cavity during laparoscopic surgery.

Once we perform conservative laparoscopic surgery, we should consider the situation of intraoperative bleeding and avoid emergency hysterectomy due to excessive bleeding during surgery. Clinical doctors evaluate intraoperative bleeding via examinations to determine the richness of blood flow signals, lesion size, and hCG values, similar to the treatment of caesarean scar pregnancy. Taking massive intraoperative bleeding into account, some researchers have implemented UAE[27] to help maintain fertility. UAE plays a vital role in decreasing bleeding and has been widely used in postpartum hemorrhage, symptomatic uterine fibroids, adenomyosis, and caesarean scar pregnancy. As UAE has become widely performed, concerns about complications have increased. Acute complications include fever, pain, nausea, vomiting, and lower limb vascular embolism. The long-term complications of UAE can include endometrial ischemic necrosis, uterine intrauterine adhesions, ovarian failure, and subsequent infertility[28]. Homer and Saridogan[29] reported that UAE is associated with an increased risk of miscarriage. Another report[30] revealed a decrease in fertility in patients who previously underwent UAE.

Compared with UAE, temporary occlusion of the uterine artery is a promising new approach that causes less postoperative pain[31] and fewer unfavorable pregnancy outcomes[32], reduces intraoperative bleeding without increasing the operative time[33] and does not influence the function of the ovary[34] since uterine artery occlusion is temporary. Li et al[35] managed intramural ectopic pregnancy with temporary aortic balloon occlusion via the femoral artery during cesarean delivery, decreasing hemorrhage, preventing blood transfusion, and maintaining fertility. Preoperative endovascular balloon occlusion can successfully prevent heavy bleeding. However, serious complications may occur, such as thrombosis, arterial pseudoaneurysms, acute lower extremity ischemia, and arterial rupture[36]. There is currently no research published on the use of uterine artery occlusion with titanium clips in the treatment of intramural pregnancy. Titanium surgical clips were first used in combination with an injection of vasopressin by Shao et al[37] to decrease uterine vascularization during the surgical excision of cesarean scar ectopic pregnancies. After that, more cases involved temporary occlusion of the bilateral uterine arteries. In another case, researchers demonstrated that a transvaginal laparoscopic procedure with temporary occlusion of the bilateral uterine arteries could terminate the cervical pregnancy[38]. Temporary occlusion of the uterine arteries is an effective strategy to avoid serious intraoperative bleeding from conditions such as uterine fibroids, uterine adenomyosis, tubal interstitial pregnancy, and cornual pregnancy. Shen et al[26] described 8 cases of intramural pregnancy treated with laparoscopic surgery or hysteroscopic surgery without preoperative intervention and reported that, in most cases, the intraoperative bleeding volume was greater than 100 mL, up to 400 mL. In our case, we temporarily occluded the bilateral uterine arteries during laparoscopic surgery to reduce intraoperative bleeding (intraoperative bleeding was approximately 20 mL) and successfully halt the progression of the pregnancy. Here, we recommend temporary occlusion of the uterine artery when the patient is at risk of excessive uterine bleeding during surgery.

Attention is needed here. Temporary occlusion of the uterine artery with titanium clips must be performed by experienced operators who are familiar with the anatomy of the pelvic organs and pelvic vessels. The operators should carefully expose the uterine artery, which is concealed and sometimes difficult to expose. By dissecting the internal iliac artery and locating the uterine artery originating from the internal iliac artery, operators can free and temporarily block the uterine artery. All operators should pay attention to the ureter and important pelvic vessels. In situations in which the uterine artery cannot be identified, causing occlusion to fail, uterine artery tears or heavy bleeding can occur, and temporarily occlusion of the internal iliac artery can be a remedial measure. There are several serious complications, including thromboembolism, lower organ ischemia and reperfusion injury, and aortic damage. The contraindications include dissecting aneurysms, substantial aortic meandering, and calcification.

Unfortunately, long-term follow-up, especially of fertility status, has not been performed in most investigations. This is also a limitation in our case. We recommend large case series studies to ascertain long-term outcomes.

Significant challenges are associated with managing intramural pregnancy. When selecting strategies for treatment, it is important to consider individual differences, particularly expectations for fertility and quality of life. Once patients with intramural pregnancy are managed, a thorough and unbiased evaluation of the benefits and drawbacks of each treatment option is essential.

CONCLUSION

We reported a case of intramural pregnancy approximately one month after medical abortion. We performed hysteroscopy and temporarily occluded the bilateral uterine arteries during laparoscopic surgery. The postoperative course was uneventful. We recommend temporary occlusion of the uterine arteries in patients at risk of excessive uterine bleeding during surgery.

ACKNOWLEDGEMENTS

We want to express our thanks to the patients, doctors, nurses, and other medical staff at Zhejiang Hospital for agreeing to participate in this study.