Cardiovasc Intervent Radiol DOI 10.1007/s00270-015-1137-9

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Spontaneous Hemoperitoneum in Pregnancy Treated with Transarterial Embolization of the Uterine Artery Takahiro Konishi1 • Kensaku Mori3 • Yoko Uchikawa1 • Sodai Hoshiai1 Masanari Shiigai4 • Rena Ohara2 • Manabu Minami3



Received: 11 March 2015 / Accepted: 11 May 2015  Springer Science+Business Media New York and the Cardiovascular and Interventional Radiological Society of Europe (CIRSE) 2015

Introduction Hemoperitoneum rarely occurs during pregnancy, except in ectopic pregnancy. Brosens et al. proposed the concept of spontaneous hemoperitoneum in pregnancy (SHiP) as unprovoked intraperitoneal bleeding during the second half of pregnancy, during labor, or occasionally during the early postpartum period [1]. Of the 25 cases reviewed, none led to maternal death. However, the perinatal mortality rate was unfavorably high at 36 % (10/28, including three sets & Takahiro Konishi [email protected] Kensaku Mori [email protected] Yoko Uchikawa [email protected] Sodai Hoshiai [email protected] Masanari Shiigai [email protected] Rena Ohara [email protected] Manabu Minami [email protected] 1

Department of Radiology, University of Tsukuba Hospital, 2-1-1 Amakubo, Tsukuba, Ibaraki 305-8576, Japan

2

Department of Obstetrics and Gynecology, University of Tsukuba Hospital, 2-1-1 Amakubo, Tsukuba, Ibaraki 305-8576, Japan

3

Department of Radiology, Faculty of Medicine, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8575, Japan

4

Department of Radiology, Tsukuba Medical Center Hospital, 1-3-1 Amakubo, Tsukuba, Ibaraki 305-8558, Japan

of twins). Diagnosis and achievement of hemostasis in maternal shock, progressive anemia, or fetal distress require emergent laparotomy. We present a woman with SHiP at 24 weeks’ gestation who was successfully treated with uterine artery embolization (UAE) for a left uterine artery aneurysm and delivered a healthy full-term baby. Case Report A 30-year-old woman (gravida 2, para 0) experienced a sudden-onset epigastric pain during sexual intercourse at 24 weeks’ gestation. Except for two spontaneous miscarriages, she had no significant medical history, including abdominal trauma or laparotomy. A local physician referred her to our hospital for further evaluation for anemia and ascites. During the physical examination, slight tachycardia (100 beats/min) without hypotension (114/73 Torr) was observed. Laboratory testing revealed anemia (hemoglobin 8.7 g/dL) and slight coagulation derangement (fibrin degradation products 5.4 lg/mL). Ultrasonography revealed a massive hyperechoic hemoperitoneum. Fetal well-being was confirmed by the obstetrician. The relatively good condition of the mother and the fetus allowed investigation of the bleeding source. Because the bleeding source, such as a splenic artery aneurysm, could be located in the upper abdomen, we determined that contrast-enhanced computed tomography (CT) of the whole abdomen would be more appropriate than pelvic magnetic resonance imaging. The patient’s consent regarding the risk of radiation exposure was obtained. According to the guideline of the American College of Obstetricians and Gynecologists, concern about the possible effects of high-dose ionizing radiation

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exposure should not prevent pregnant women from undergoing medically indicated diagnostic radiographic procedures [2]. In addition to massive hemoperitoneum, a saccular aneurysm (17 mm in diameter) was identified in the trunk of the left uterine artery (Fig. 1). Higher attenuation of the hemoperitoneum in the left lower abdomen suggested that the aneurysm was the bleeding source despite the lack of extravasation. Two therapeutic options were presented, namely primary surgical hemostasis and UAE with surgical standby. After receiving information about possible complications, including miscarriage, the patient opted for UAE because it is less invasive. The procedure was performed with standby gynecologists in our hybrid operating room,

where an interventional radiographic system (Allura Clarity FD 20, Philips Medical Systems, Best, The Netherlands) is seamlessly integrated with the operating room table (Magnus, Maquet GmbH, Rastatt, Germany). Under local anesthesia, a 4-F Cobra catheter was inserted in the left internal iliac artery by using the right femoral approach. A 2.3-F microcatheter (Prowler Select Plus, Johnson and Johnson, New Brunswick, NJ, USA) was advanced into the left uterine artery, where we embolized the aneurysm using the isolation technique. However, the aneurysm ruptured when we embolized the uterine artery distal to the aneurysm by using four mechanically detachable coils up to 4 mm in diameter and 15 cm in length (Interlock, Boston Scientific, Cork, Ireland) and

Fig. 1 A Precontrast computed tomography (CT) scan showing the massive hemoperitoneum and the fetus within the uterus. The hemoperitoneum density was higher in the left lower abdomen than in the right lower abdomen (arrows). B Arterial-phase CT image showing nodular enhancement in the partially thrombosed aneurysm

(arrows). C Delayed phase CT image showing peripheral curvilinear enhancement in the partially thrombosed aneurysm (arrows). D Maximum intensity projection of the arterial-phase CT showing nodular enhancement on the descending portion of the left uterine artery (arrow)

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three pushable coils (Tornado, Cook Medical, Bloomington, IN, USA). Therefore, we embolized the ruptured aneurysm with a mixture of 17 % n-butyl cyanoacrylate (NBCA; Hystacryl, B. Braun, Melsungen, Germany) and iodized oil (lipiodol; Guerbet, Aulnay-sous-Bois, France). Subsequently, we embolized the uterine artery proximal to the aneurysm using two pushable metallic coils (Tornado). However, extravasation appeared from the tear of the proximal uterine artery that required an additional injection of NBCA–lipiodol. Finally, left internal arteriography revealed the embolized left uterine artery from its origin and no further extravasation (Fig. 2). The exposed dose was 2111.2 mGy cm (dose-length product) for CT, and the air kerma was 1085.58 mGy for 33.4 min for angiography. The volumes of the contrast media used were 100 and 45 mL, respectively.

Fig. 2 A Left internal iliac arteriogram showing the left uterine artery aneurysm before the endovascular procedure (arrow). B Selective left uterine arteriogram showing the aneurysm (arrow). C The aneurysm ruptured after coil embolization of the distal side (arrow),

After the procedure, the patient recovered uneventfully. Obstetric examinations revealed no fetal complications. The patient continued her pregnancy and returned to regular prenatal checkups. The patient delivered a healthy female baby transvaginally at 41 weeks 3 days of pregnancy. She recovered from atonic hemorrhage, perineal laceration, and eclampsia without significant sequelae. Histopathological examination revealed no UAE-related ischemic changes or infarctions in the placenta.

Discussion According to the aforementioned review of 25 SHiP cases [1], hemorrhages originate from veins, arteries, and unknown locations in 80 % (20/25), 16 % (4/25), and 4 % (1/

with extravasation (arrowheads). D Final left internal iliac arteriogram showing the complete occlusion of the proximal left uterine artery from its origin, including the aneurysm with coils and n-butyl cyanoacrylate–lipiodol (arrows)

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25) of cases, respectively. As arterial causes are less common, surgery rather than UAE is normally the first treatment choice for SHiP, especially in cases of maternal shock or fetal distress. In the present case, the patient’s relatively stable condition allowed us to determine the bleeding source and perform endovascular treatment. Surgical conversion is considered in case of embolization failure or sudden deterioration. The cause of the arterial hemorrhage in SHiP is unclear, but studies suggest that surgical procedures induce vascular damage and pseudoaneurysm formation. In this case, however, the patient had no history of surgery, trauma, traumatic deliveries, or endometriosis. Her aneurysm can be considered a true aneurysm. In our literature search, we found only three case reports regarding UAE for uterine artery aneurysm during pregnancy. The details of these cases [3–5] and ours are listed in Table 1. UAE was performed in the second or third trimester in all the patients. Our case is the second reported case of SHiP treated with UAE, preceded only by the case reported by Gavanier et al. in 2012 [5]. Unlike in our case, the aneurysms in the other three cases are considered pseudoaneurysms.

The true aneurysm reported by Gavanier et al. could have been a false aneurysm because the patient had a history of ipsilateral oophorectomy and cesarean section [5]. In three of four cases of uterine artery aneurysm, unilateral UAE resulted in successful hemostasis. In these three cases, coils with or without NBCA–lipiodol were used to preserve peripheral collateral flow and all patients continued their normal pregnancies until delivery. In the remaining case, vaginal bleeding recurred [3]. Although the authors considered the rebleeding to be caused by placental abruption, the actual cause might have been rerupture. In this case, embolic particles (250–355 lm in diameter) were used in addition to coils. We do not recommend the use of particles because these may cause uterine ischemia by blocking the distal flow beyond the collateral arterial supplies. In addition, when placing the first coil, a detachable coil might be preferred to a free coil, as a free coil may lodge more distally than expected, as in our case. Blood flows higher in uterine arteries during pregnancy. We recommend distal protection by using coils before infusing NBCA–lipiodol, as its effects on the placenta and fetus are unclear.

Table 1 Uterine artery embolization during pregnancy First author (publication year)

Laubach (2000) [3]

Cornette (2014) [4]

Gavanier (2012) [5]

Konishi (present)

Age (year)/gravida/para

33/1/0

37/2/1

36/2/1

30/2/0

Gestational age (weeks)

28

27

20

24

Bleeding site

Vaginal

Vaginal

Intraperitoneal

Intraperitoneal

Previous pelvic surgery

Laparoscopic surgery for endometriosis

Laparoscopic appendectomy

Cesarean section

None

Endometriosis Source of bleeding

Yes Uterine artery pseudoaneurysm

Yes Uterine artery pseudoaneurysm

Yes Uterine artery pseudoaneurysma

No Uterine artery true aneurysm

Imaging modality for diagnosis

MR angiography

Contrast-enhanced MR imaging

Contrast-enhanced CT

Contrast-enhanced CT

Embolized uterine artery Embolic material

Unilateral

Unilateral

Unilateral

Unilateral

Coils

Oophorectomy

Coils

Particles

Coils

Coils

Mixture of NBCA and iodized oil

Hemostasis by embolization

Unknownb

Yes

Yes

Fetal complication?

Premature birth

None

None

None

Delivery

Emergent cesarean section at 30 weeks

Elective cesarean section at 37 weeks

Elective cesarean section at 34 weeks

Transvaginal delivery at 41 weeks

Mixture of NBCA and iodized oil Yes

MR magnetic resonance, CT computed tomography, NBCA n-butyl cyanoacrylate a

Although the authors described a true aneurysm of the uterine artery as the bleeding source, a pseudoaneurysm was more likely because the patient underwent ipsilateral oophorectomy and cesarean section

b

Although vaginal bleeding recurred 5 days post embolization, the authors suggested that placental abruption was the cause

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In conclusion, we encountered a rare case of SHiP successfully treated with unilateral and proximal UAE for a uterine artery aneurysm. When maternal and fetal conditions are good, the bleeding source can be investigated. For arterial bleeding in SHiP, proximal UAE is a safe and definitive treatment. However, we emphasize that the endovascular procedure should be performed with standby gynecologists in case quick surgical conversion is required. Conflict of interest All authors declare no conflicts of interest associated with this manuscript. Statement of Informed Consent Informed consent was obtained from the patient. Statement of Human and Animal Rights This article does not contain any studies with human or animal subjects.

References 1. Brosens IA, Fusi L, Brosens JJ. Endometriosis is a risk factor for spontaneous hemoperitoneum during pregnancy. Fertil Steril. 2009;92(4):1243–5 (Epub 2009 May 12). 2. American College of Obstetricians and Gynecologists. Guidelines for diagnostic imaging during pregnancy. ACOG Committee Opinion No. 299. Obstet Gynecol. 2004;104:647–51. 3. Laubach M, Delahaye T, Van Tussenbroek F, Debing E, De Catte L, Foulon W. Uterine artery pseudo-aneurysm: diagnosis and therapy during pregnancy. J Perinat Med. 2000;28(4):321–5. 4. Cornette J, Wilk E, Janssen NM, Weiden RMF, Jenninkens SFM, Pattynama P, Duvekot JJ. Uterine artery pseudoaneurysm requiring embolization during pregnancy. Obstet Gynecol. 2014;123(2 Pt 2 Suppl 2):453–6. 5. Gavanier D, Orsoni M, Dupuis O, Valette PJ. Spontaneous hemoperitoneum during pregnancy and uterine artery aneurysm. Gynecol Obstet Fertil. 2012;40(11):711–4 (Epub 2012 Oct 23).

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Spontaneous Hemoperitoneum in Pregnancy Treated with Transarterial Embolization of the Uterine Artery.

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