Surgical Resection with Uterine Preservation in Uterine Arteriovenous Fistula: A Case Report and Literature Review

Abstract

Background:

Uterine arteriovenous fistula (UAVF), a rare condition, usually occurs in females of reproductive age and is commonly diagnosed in those with histories of myometrial traumas. UAVF is generally associated with severe bleeding. Treatment choices are usually limited to selective embolization or hysterectomy; however, other treatment options—such as surgical occlusion of the pelvic vessels, and, less frequently, en bloc resection of the lesion adjacent to the surrounding myometrium with uterine reconstruction—have also been reported. This article presents a case of conservative surgical management (CSM) of the condition, with details about a simple surgical technique and a literature review on this topic.

Case:

A 25-year-old female (gravida 1, molar 1), with a history of curettage 11 months before consultation, presented with severe vaginal bleeding and severe anemia. UAVF was diagnosed based on findings of Doppler ultrasound and magnetic resonance angiography. This patient was managed with complete surgical resection of the UAVF and uterine reconstruction.

Results:

Remarkably, this patient had a spontaneous pregnancy 15 months' postoperatively.

Conclusions:

A review of the literature identified only 5 reports on CSM, with the most frequently used treatments being hysterectomy and arterial embolization for UAVF. The former method eliminates all possibilities of future pregnancies, whereas the latter has a high failure rate for the first attempt. In cases of UAVF in which fertility preservation is preferred and expectant management is not possible, surgical resection of the affected area followed by uterine reconstruction represents a valid option for health care centers with experienced interdisciplinary teams.

Introduction

Uterine arteriovenous fistula (UAVF) is a rare condition, but it is considered potentially life-threatening, owing to the possibility of causing severe hemorrhage.

Most cases of UAVF occur during the reproductive years of females, and almost all cases to date have been reported in females with histories of curettage,¹ cesarean section, or other types of trauma. Although UAVF is rare, with only 100 cases reported until 2011,² it can cause severe vaginal bleeding³ and should be considered as a cause of late postpartum hemorrhage.

The differential diagnoses of UAVF includes retained products of conception, gestational trophoblastic disease, endometrial polyps, and vascular neoplasms, as well as all entities with localized increases of uterine vascularization and arteriovenous short circuits noted on ultrasound (US).⁴ The diagnosis is made using Doppler US and must be differentiated from the diagnosis of retention of placental remnants because UAVF is associated with massive bleeding when endometrial curettage is performed.⁵

Treatment is usually limited to selective embolization or hysterectomy, although en bloc resection adjacent to the surrounding myometrium and selective coagulation have also been described.

This article presents the case of a woman with surgically managed UAVF who underwent a complete surgical resection of the malformation followed by a spontaneous pregnancy. In addition, the article presents a literature review on this subject.

Case

A 25-year-old female was gravida 1, molar 1. This patient's molar pregnancy was treated with curettage, resulting in a loss of the ß-subunit of human chorionic gonadotropin (ß-hCG). Following postcurettage at 11 months, the patient reported severe vaginal bleeding that lasted for 2 weeks, and was hospitalized for testing and treatment.

A US examination revealed a 23 × 28 mm intramyometrial mass located on the left uterine isthmus at a distance 2 mm from the endometrial cavity. The mass had an obvious flow detected by Doppler US and a jet flow corresponding to arterial flow (Fig. 1). Furthermore, magnetic resonance angiography revealed an intramyometrial vascular nest with multiple anastomoses between the branches of both uterine arteries and other branches corresponding to the collaterals of the internal iliac arteries. Based on these findings, UAVF was diagnosed, and the size of the mass indicated a high risk of rupture and the possibility of severe bleeding. Considering the large size of this mass and its multiple collaterals, the use of endovascular management was eliminated. On the patient's second hospitalization day, her vaginal bleeding increased and her hemoglobin level decreased from 9 dL to 7 g/dL. Accordingly, conservative treatment comprising surgical resection of the malformation was proposed, considering the patient's desire for fertility preservation. Upon completion of laparotomy, although the lesion was not evident on inspection, it was evident on palpation of the left side of the isthmus.

FIG. 1.

(A) Sagittal ultrasound scan, left paramedian of the uterus: rounded hypoechoic lesion measuring 21 × 27 mm, with arterial flow jet (arrow). (B) Color Doppler applied on a hypoechoic lesion, with identification of pulsatile flow from the arterial vessel, filling the cavity described in A. (C) Three-dimensional reconstruction of magnetic resonance angiography showing vascular mass (arrow) with blood supply from both uterine arteries and other branches of the internal iliac arteries. Right external iliac artery (arrowhead). Color images are available online.

The following surgical steps were undertaken for the resection of the fistulous mass: (1)

Wide dissection of the vesicouterine area to expose the entire uterine anterolateral surface of the uterus

(2)

Identification of the UAVF on palpation and confirmation via US

(3)

Vascular isolation of the malformation using hemostatic sutures in four quadrants (Figs. 2 and 3)

(4)

Total resection of the UAVF and part of the surrounding myometrium

(5)

Identification of the cervical canal and endometrial cavity, using a plastic catheter prior to performing uterine closure

(6)

Hysterorrhaphy using separate square stitches (Figs. 2 and 4).

FIG. 2.

Anterior view of the uterus after dissection of the vesicouterine space. (A) Delineation of the arteriovenous fistula (yellow line) and location of the hemostatic points in 4 quadrants (medial, lateral, superior, and inferior) to the uterine arteriovenous fistula (UAVF; red lines). (B) Lateral hemostatic point placed, making evident the bulging in the anterior wall of the uterus produced by UAVF blood congestion. (C) Resection of the UAVF, vascular cavity opening of 28 mm. (D) Reconstructed uterus after resection of the UAVF. Suture of the hysterorrhaphy second layer is shown. Color images are available online.

FIG. 3.

Illustration of the hemostatic sutures' positions on the four quadrants, limiting vascular flow toward arterio (red) venous (blue) fistula. Color images are available online.

FIG. 4.

(A) Surgical specimen: 3 × 4–cm lesion, consisting of multiple vessels that flow into (arrow) a 2.5-cm diameter cavity. (B) Orcein coloration: proliferation of thick-walled vessels in the thickness of the myometrium, highlighted by the orcein coloration that shows the reticular fibers of the vascular walls (asterisks). (C) Masson's trichrome coloration: Proliferation of thin-(probably veins, marked with arrows) and thick-walled vessels (of an arterial nature, marked with an asterisk), in close contact. (D) Hematoxylin and eosin stain: presence of nerve branches adjacent to the vessels (arrow). Color images are available online.

The patient's informed consent was obtained for this procedure.

Results

Intraoperative bleeding of 100 cc was estimated, and the total surgical time was 90 minutes, with no surgery-related complications. A subdermal implant was inserted as a contraceptive method for 14 months, and the patient was discharged on the second postoperative day. Follow-up US testing, performed at 3 weeks and at 14 months following discharge, revealed normal uterine vasculature. Similarly, follow-up hysterosalpingography and hysteroscopy revealed normal findings; hence, the subdermal implant was removed. One month later, the patient had a spontaneous pregnancy but had an incomplete abortion at 8 weeks, which was managed with vacuum curettage with no complications.

Discussion

A database search was conducted using PubMed, OVID, and SciELO for studies published between 1990 and 2017 using the terms uterine arteriovenous malformation and uterine arteriovenous fistula. Case studies, case series, and review articles were included, primarily aiming at identifying patients managed with surgical resection of the malformation and subsequent uterine reconstruction. In total, 403 results were obtained during the initial search. After an initial review, 222 bibliographical references were selected, 42 of which corresponded to case series and 3 to systematic reviews. The other articles were case reports.

In 5 references, CSM was reportedly used (Table 1) for patients with histories of uterine traumas or gestational trophoblastic disease and who wished to achieve pregnancy in the future. In 2 cases, arterial embolization resulted in repeated failures. Furthermore, the affected area was resected in 1 patient because it was a gestational trophoblastic tumor. In 2 cases, the size and number of arterial anastomoses predicted a possible failure of pelvic vessel embolization (PVE). In fact, only 1 full-term pregnancy was reported following CSM.⁶ In the other cases, hysterectomy was performed.

Table 1.

Previous Publications of Patients with UAVF Managed with Surgical Resection & Uterine Preservation (CSM)

1st Author, year, ref. & country	Patient's clinical characteristics	Surgery type	Results	Blood loss in surgery	PVE previous attempt	Subsequent pregnancy
Patton, 2015,²⁹ United States	Age 34, gravida 3, para 1, cesarean 1, abortions 2; vaginal bleeding 3 months after curettage; hCG negative; 3.8-cm lesion in the anterior uterine body	Programmed laparoscopy; ligature of both uterine arteries; resection of AVM & hysterorrhaphy	Absence of AVM on resonance imaging 8 months after resection	300 mL	PVE on two occasions with recurrence of symptoms and recanalization of AVM	Not reported
Chen, 2013,²⁶ China	Age 36, gravida 3, para 1, cesarean 1, abortions 2; 10-month hypermenorrhea, 2 transfusions for massive bleeding, hCG 0.1 IU/L; 5.3 × 4.5 × 3.1–cm lesion in the lower segment of the anterior, posterior & bilateral walls of the uterus	No UAE; programmed laparoscopy; resection of uterine AVM & hysterorrhaphy	Symptoms disappear, but uterine adhesion with amenorrhea occurs at 5-month follow-up	80 mL	PVE not considered a definitive therapeutic option because of extensive nature of the lesion & the multiple uterine segments involved	Not reported
Rygh, 2009,²⁷ Norway	Age 22, gravida 2, para 1, molar 1; abnormal bleeding 2 months after curettage; hCG 3 IU/L; 5.5 × 3.5–cm lesion on the front of the isthmus	Emergency laparotomy; resection of affected segment of uterus & hysterorrhaphy	Absence of uterine AVM on US 6 weeks after resection; normal menstruation	Not reported	Embolization of both uterine arteries; rebleeding 6 days after PVE; in second embolization, branches of uterine, ovarian, & internal pudendal arteries approached; patient bled again 4 days later	Not reported
Corusic, 2009,²⁸ Croatia	Age 21, primigravida, with invasive trophoblastic disease managed with D&C, followed by chemotherapy; monitoring US after 4th cycle of methotrexate; a hypervascularized lesion of 5 × 3.3 × 3.2 cm on back wall of uterus	Programmed laparoscopy; resection of affected area, including resection of the fallopian tube & round ligament	Absence of AVM on US 12 months after resection; Normal menstruation 2 months after chemotherapy	50 mL	Not considered	Not reported
Nikolopoulos, 2004,⁶ United Kingdom	Age 39, gravida 1, abortion 1; heavy vaginal bleeding 2 months after curettage required transfusion; lesion on left wall of uterus; arteriography with anastomosis of bilateral ovarian & left uterine arteries	Programmed laparotomy; ligation of vessels involved in the lesion; Surgical resection of affected area	Absence of AVM on US 9 months after resection; normal menstruation	Not reported	PVE considered not viable due to the size & number of vessels irrigating the AVM	Spontaneous pregnancy 14 months later, with cesarean & product of 3010 g

CSM, conservative surgical management; hCG, human chorionic gonadotropin; IU, international units; D&C, dilatation and curettage; US, ultrasound; UAE, uterine arterial embolization; AVM, arteriovenous malformation; PVE, pelvic vessels embolization

Although hysterectomy represents definitive management, it implies the impossibility of future pregnancy. On the other hand, PVE requires a high level of specialization and involves risks, with possible complications such as those associated with arterial puncture and ovarian insufficiency.⁷ PVE can also result in unwanted embolization with catastrophic consequences due to the passage of embolization materials into the kidneys, lungs, and brain.⁸

PVE is a minimally invasive technique and usually facilitates the identification of the vessels involved, but recurrences are frequently reported.⁹ The primary success rate of PVE is reportedly 61%¹⁰ and is related to the surgeon's technique and experience, given that the uterus has a complex vascular supply¹¹ with additional supplying from the bladder and vaginal vessels, apart from those conventionally considered (uterine and gonadal vessels). This explains the inherent difficulty of endovascular management.¹²

Some surgeons resort to surgical vascular ligation^13–16 when confronted with repeated failures of PVE or when failure is predicted owing to an extensive network of arterial anastomoses; but hysterectomy is generally considered a preferred solution.

Therefore, the possibility of a second or third endovascular procedure is considered essential, along with additional therapeutic methods that facilitate fertility preservation. In this regard, few options are currently available. On the one hand, expectant management is another option for spontaneous regression; this approach is taken in up to 50% of cases,¹⁷ particularly in cases of patients with asymptomatic UAVFs.^18,19 Alternatively, it has been reported that use of the oral contraceptives methylergonovine,²⁰ danazol,²¹ progesterone, or methotrexate²² have led to the disappearance of these lesions.²³

The situation changes when a patient presents with active bleeding or hemodynamic instability, because expectant management is not feasible. In this case, the conventional option is hysterectomy even in centers with experience in UAVF management,²⁴ but CSM gains value if fertility preservation is preferred. This procedure, although not included in flow charts²⁵ and rarely reported in the literature (Table 1), is technically simple when the lesions are not very extensive (Fig. 3).

To date, only 5 reports of patients with UAVF undergoing CSM have been published (Table 1).^6,26–29 The current patient had severe bleeding and severe anemia, requiring immediate intervention. The complexity of the arterial anastomoses related to the lesion (Fig. 1) eliminated the possibility of performing PVE for initial management, with surgical resection of the vascular lesion being performed successfully. As a hemostasis strategy, some researchers have performed arterial ligation prior to resection.^6,26 The current authors' technique included placement of hemostatic sutures in four quadrants around the lesion (Fig. 3), enabling the achievement of hemostasis by resecting an ∼3-cm vascular nest (Figs. 2 and 4). Although this patient's lesion was relatively smaller than those reported previously, CSM has been reported to be useful against lesions of up to 5 cm.²⁶

Although this patient had a history of a molar pregnancy, her ß-hCG had become negative 10 months before the UAVF was identified, and histologic examination of the lesion, enabled by the primary use of PVE, eliminated the possibility of her having trophoblastic tissue. (Fig. 4). For cases in which positive chorionic gonadotropin is identified, a gestational trophoblastic tumor must be ruled out before intervention.³⁰

Following PVE for the management of UAVF, pregnancies have been reported in 53% of patients.²⁰ The results of patients following CSM have been reported rarely (Table 1), with only 1 reported full-term pregnancy⁶ and the current case being the second one, although it resulted in an incomplete abortion at gestational 8 weeks.

Conclusions

Although the important role of interventional radiology and endovascular management of UAVF cannot be denied, its technical difficulty and possible complications must influence its inclusion among other management options. In selected cases of patients with the desire to preserve fertility, the need for definitive management—and without the option of conservative management—surgical resection of the affected area followed by uterine reconstruction represents a valid option at healthcare centers with experienced interdisciplinary teams.

Footnotes

Acknowledgment

The authors thank the Clinical Research Center of the Fundación Valle del Lili, Cali, Colombia, for the collaboration and advice during the work on this report.

Author Disclosure Statement

No financial conflicts of interest exist.

References

Lalitha

, Seetha

, Shanmugasundaram

, Rajendiran

. Uterine arteriovenous malformation: Case series and literature review. J Obstet Gynecol India, 2016; 66:282.

Peitsidis

, Manolakos

, Tsekoura

, Kreienberg

, Schwentner

. Uterine arteriovenous malformations induced after diagnostic curettage: A systematic review. Arch Gynecol Obstet, 2011; 284:1137.

Sato

, Nakayama

, Nakamura

, Ishikawa

, Katagiri

, Kyo

. A case with life-threatening uterine bleeding due to postmenopausal uterine arteriovenous malformation. BMC Womens Health, 2015; 15:10.

Goyal

, Goyal

, Mahajan

, Sharma

, Dev

. Acquired uterine arteriovenous malformation developing in retained products of conception: A diagnostic dilemma. J Obstet Gynaecol Res, 2014; 40:271.

Scribner

, Fraser

. Diagnosis of acquired uterine arteriovenous malformation by Doppler ultrasound. J Emerg Med, 2016; 51:168.

Nikolopoulos

, Murray

. Successful pregnancy outcome after surgical removal of arteriovenous malformation of the uterus. J Obstet Gynaecol, 2004; 24:315.

Mekaru

, Oishi

, Akamine

, Heshiki

, Aoki

. Spontaneous regression of uterine arteriovenous malformations with conservative management. Case Rep Obstet Gynecol, 2017; 2017:6437670.

Fatal nontarget embolization via an intrafibroid arterial venous fistula during uterine fibroid embolization. J Vasc Interv Radiol, 2009; 20:419.

Vilos

, Vilos

, Hollett-Caines

, Oraif

, Garvin

, Kozak

. Uterine artery embolization (UAE) for uterine arteriovenous malformation (AVM) in 5 women desiring fertility: Pregnancy outcomes. J Minim Invasive Gynecol, 2015; 22(6[,suppl]):S234.

10.

Yoon

, Jones

, Taani

, Buhimschi

, Dowell

. A systematic review of acquired uterine arteriovenous malformations: Pathophysiology, diagnosis, and transcatheter treatment. AJP Rep, 2016; 6:e6.

11.

Palacios Jaraquemada

, García Mónaco

, Barbosa

, Ferle

, Iriarte

, Conesa

. Lower uterine blood supply: Extrauterine anastomotic system and its application in surgical devascularization techniques. Acta Obstet Gynecol Scand, 2007; 86:228.

12.

Kishino

, Miyasaka

, Takeguchi

, Ohashi

. Retrograde transvenous obliteration for uterine arteriovenous malformation. Obstet Gynecol, 2014; 123:427.

13.

Raherinantenaina

, Rajaonanahary

TMA

, Randriamandrato

TAV

, Rakoto Ratsimba

. Acquired uterine arteriovenous malformation successfully treated with selective ligation of the internal iliac artery. J Mal Vasc, 2015; 40:182.

14.

Levy-Zaubermann

, Capmas

, Legendre

, Fernandez

. Laparoscopic management of uterine arteriovenous malformation via occlusion of internal iliac arteries. J Minim Invasive Gynecol, 2012; 19:785.

15.

Milingos

, Doumplis

, Sieunarine

, Savage

, Lawson

, Smith

. Uterine arteriovenous malformation: Fertility-sparing surgery using unilateral ligation of uterine artery and ovarian ligament. Int J Gynecol Cancer, 2007; 17:735.

16.

, Liu

, Yuan

, Ng

. Successful treatment of symptomatic arteriovenous malformation of the uterus using laparoscopic bipolar coagulation of uterine vessels. Fertil Steril, 2001; 76:1270.

17.

Timmerman

, Van den Bosch

, Peeraer

, Debrouwere

, Van Schoubroeck

, Stockx

, et al. Vascular malformations in the uterus: ultrasonographic diagnosis and conservative management. Eur J Obstet Gynecol Reprod Biol. 2000 Sep; 92(1):171–8.

18.

JKY

, Cheung

VYT

, Khongsni

. Management and outcome of sonographically diagnosed uterine enhanced myometrial vascularity/arteriovenous malformations following early pregnancy events: A single center experience. Med Ultrason, 2016; 18:403.

19.

Dar

, Karmin

, Einstein

MH.Z

. Arteriovenous malformations of the uterus: Long-term follow-up. Gynecol Obstet Invest, 2008; 66:157.

20.

Eling

, Kent

, Robertson

. Pregnancy after uterine arteriovenous malformation—case series and literature review. Australas J Ultrasound Med, 2012; 15:87.

21.

Takeuchi

, Yamada

, Iwasa

, Maruo

. Successful medical treatment with danazol after failed embolization of uterine arteriovenous malformation. Obstet Gynecol, 2003; 102:843.

22.

Vaknin

, Sadeh-Mefpechkin

, Halperin

, Altshuler

, Amir

, Maymon

. Pregnancy-related uterine arteriovenous malformations: Experience from a single medical center. Ultraschall Med, 2011; 32(suppl2):E92.

23.

Oride

, Kanasaki

, Miyazaki

. Disappearance of a uterine arteriovenous malformation following long-term administration of oral norgestrel/ethinyl estradiol. J Obstet Gynaecol Res, 2014; 40:1807.

24.

Kim

, Kim

, Do

, et al. Surgical treatment for congenital arteriovenous malformation: 10 years' experience. Eur J Vasc Endovasc Surg, 2006; 32:101.

25.

Ishihara

, Kanasaki

, Oride

, Hara

, Kyo

. Differential diagnosis and management of placental polyp and uterine arteriovenous malformation: Case reports and review of the literature. Womens Health (Lond), 2016; 12:538.

26.

Chen

S-Q

, Jiang

H-Y

, Li

J-B

, Fan

, Liu

M-J

, Yao

S-Z

. Treatment of uterine arteriovenous malformation by myometrial lesion resection combined with artery occlusion under laparoscopy: A case report and literature review. Eur J Obstet Gynecol Reprod Biol, 2013; 169:172.

27.

Rygh

, Greve

, Fjetland

, Berland

, Eggebø

. Arteriovenous malformation as a consequence of a scar pregnancy. Acta Obstet Gynecol Scand, 2009; 88:853.

28.

Corusic

, Barisic

, Lovric

, Despot

, Planinic

. Successful laparoscopic bipolar coagulation of a large arteriovenous malformation due to invasive trophoblastic disease: A case report. J Minim Invasive Gynecol, 2009; 16:368.

29.

Patton

, Moy

, Milad

, Vogezang

. Fertility-preserving management of a uterine arteriovenous malformation: A case report of uterine artery embolization (UAE) followed by laparoscopic resection. J Minim Invasive Gynecol, 2015; 22:137.

30.

, Yi

, Sohn

, Lee

. Acquired uterine vascular abnormalities associated with persistent human chorionic gonadotropin: Experience at a Korean teaching hospital. Taiwan J Obstet Gynecol, 2015; 54:654.