Uterine arteriovenous malformation (AVM) is a rare disease characterized by abnormal communication between the uterine arteries and the myometrial veins. AVM can be congenital or, more commonly, acquired [1]. Although rare, uterine AVM is potentially life-threatening because of the massive bleeding it can cause. In the past, the treatment of choice was hysterectomy. A more conservative approach with uterine artery embolization is now preferred, particularly in premenopausal women who are willing to preserve fertility [2].

We present the case of a patient with a congenital AVM treated with uterine arteries embolization by means of contour emboli at the age of 7 months, who developed vaginal bleeding at the ages of 13 and 14 years. We describe the radiological re-embolization of a congenital AVM nidus in a young girl performed twice (with an interval of one year) by means of a liquid embolizing agent, commonly used for intracranial AVMs.

Figure 1. (a) Axial T2-weighted MRI image showing hypointense and serpiginous bilateral tubular structures (see arrows) corresponding to the aberrant vascular structures of the arteriovenous malformation of the uterine cervix. (b) Post-contrast axial T1-weighted fat-suppressed image showing the intense enhancement of the malformation.

In October 2010, a 13-year-old girl was admitted to the Pediatrics Department for vaginal bleeding. The patient, who had menarche in September 2010, had a congenital uterine AVM treated at the age of 7 months with polyvinyl alcohol embolization (Contour, Boston Scientific, Natick, MA, USA). The patient had two previous vaginal bleeding episodes that resolved spontaneously, one in 2002 and one in July 2010. At admission, the patient was hemodynamically stable, thus no blood transfusions were administered. The vaginal bleeding stopped within 5 hours from the admission, after tranexamic acid per os (Ugurol, Rottapharm S.p.A., Milan, Italy). Pelvic US (not shown) and MRI (Figure 1) confirmed the diagnosis of AVM in the uterine cervix. The patient was discharged and two weeks later she was re-admitted for uterine arteries embolization procedure, after obtaining written informed consent (by her parents also).

Figure 2. (a, b) Aortoiliac digital subtraction angiography and selective right uterine artery angiography showing the multiple abnormal vascular connections constituting the arteriovenous malformation, with prevalent left venous drainage. (c) Selective right uterine artery angiography after embolization with Onyx and coils (see arrows), showing partial devascularisation of the nidus.

Through left common femoral artery access, an aortoiliac digital subtraction angiography confirmed the AVM (Multistar D, Siemens, Erlangen, Germany). With a 2D roadmapping technique, selective catheterization of both uterine arteries was performed by means of a 5F catheter sheath (Cobra 2, Terumo Interventional Systems, Somerset, NJ). A liquid embolizing agent (ethilene vinyl-alcohol copolymer, Onyx, Ev3, Irvine, CA, USA) and coils (Interlock – 35 Fibered IDC Occlusion System, Boston Scientific, Natick, MA, USA) were injected in the uterine arteries, with partial devascularisation of the nidus (Figure 2). The procedure time was 64 minutes and the skin dose to the patient was 620 mGy.

At discharge, haemoglobin and ematocrit were normal.

Figure 3. (a) Axial T2-weighted MRI image showing that the arteriovenous malformation was markedly enlarged if compared to Figure 1, occupied the cervix and was extended to the body of the uterus and the proximal vagina. (b) Coronal Maximum Intensity Projection reconstruction of the Angio-MR sequence demonstrating that the nidus had a communication with the hemorrhoidal plexus.

At pelvic US and MRI performed one month after the procedure (not shown), the AVM showed no significant modifications. The patient was asymptomatic in the following months, thus no other pelvic USs or MRIs were performed, as the patient wished.

In December 2011, the patient developed once more vaginal bleeding, thus she was re-admitted to the Pediatrics Department. The patient was hemodynamically stable, thus tranexamic acid was given per os and the bleeding stopped within 3 hours from admission. Pelvic US (not shown) showed that the AVM nidus was enlarged, if compared to the latest US examination. Pelvic MRI confirmed the US findings, and the Angio-MR sequence showed also that the nidus had a communication with the hemorrhoidal plexus and was extended to the body of the uterus and the proximal vagina (Figure 3). The embolization procedure was performed the same day of the MRI examination, after written informed consent, injecting only ethilene vinyl-alcohol copolymer in both uterine arteries with again partial devascularisation of the nidus (Figure 4). The procedure time was 56 minutes and the skin dose to the patient was 580 mGy.

Figure 4. (a, b) Aortoiliac digital subtraction angiography and selective left uterine artery angiography showing that the AVM was significantly enlarged if compared to Figure 2. (c) Selective right uterine artery angiography after embolization with Onyx, showing partial devascularisation of the nidus.

In July 2012, the patient underwent follow-up MRI (not shown) that showed a slight enlargement of the AVM. No bleeding had occurred between December 2011 and March 2014.

Uterine AVM is believed to be a rare condition; however, its real incidence is unknown [3]. Most cases are described in women between 20 and 40 years of age. The congenital lesions are thought to be caused by alteration of the correct embryologic development of the vessels, resulting in the absence of the capillary bed between arteries and veins, with multiple abnormal vascular connections. The acquired forms can follow various pathological conditions such as surgical procedures on the uterus, infections, first trimester pregnancy loss, trophoblastic disease, caesarean scar pregnancy, trauma; they usually consist of a single large arteriovenous lesion [4] [5] [6] [7] [1]. AVM can be asymptomatic, but also be responsible for recurrent abortions and life-threatening vaginal bleeding [3].

In the past, the treatment of choice was hysterectomy, however the age of the patient and fertility preservation should be taken into consideration. For these reasons, uterine arteries embolization is now preferred for AVM management. In the international literature there are reports concerning the endovascular treatment of uterine AVMs, with subsequent successful pregnancies and deliveries [2] [7] [8]. Various embolic materials are used, such as poly-vinyl alcohol particles, embospheres, gelatin sponge, coils, n-butyl cyanoacrylate, gelfoam pledgets, both alone and in combination [1] [2] [3] [6] [7] [8] [9].

Ethilene vinyl-alcohol copolymer is a liquid embolic agent. It is commercially available mixed with dimethil-sulfoxide (an organic solvent) and micronized tantalium powder (for radiographic evaluation) under the name of Onyx. It has been used mainly for intracranial arteriovenous malformations since the 1990s, and more recently in other lesions such as pancreatic and hepatic arteriovenous malformations [10] [11], visceral arteries aneurysms and pseudoaneurysms [12], peripheral vascular malformations [13], bleeding in pancreatitis [14]. Onyx has nonadhesive proprieties, so it does not glue the catheter tip and it is possible to stop and assess the embolization process while performing it. This allows a very controlled procedure. Moreover, it is nonabsorbable, thus it produces permanent vascular occlusion [15]. These favourable features met the need we had, in this particular patient, to perform a thorough procedure without losing control of the embolizing agent administration at any time. Unfortunately, the patient experienced vaginal bleeding after one year from the first procedure, but we did not encounter any difficulty in performing the embolization with Onyx again. We did not have any complication or adverse effect during or soon after the two embolizations.

We considered the use of ethilene vinyl-alcohol copolymer as appropriate in this patient, since we were able to perform controlled procedures with subsequent symptom resolution. However we are aware that, due to the facts that bleeding occurred again and in the interval time the nidus enlarged, our procedures will probably be effective only temporarily. In our opinion, the goal of the radiological procedures in this particular patient should only be to postpone hysterectomy as long as possible, as the patient (and her parents) strongly wishes. Given the patient's age, radiation dose is always of concern, also because multiple interventions over time are expected. Up to now, the total skin dose administered in this case is 1.2 Gy, but it could grow over time and compromise a physiologic pregnancy, if ever possible in this young girl.

In year 2002, the use of Onyx has been described for the embolization of two large AVMs [16]. The liquid embolizing agent has been used also more recently in combination with n-butyl cyanoacrylate and gelatine sponge in the treatment of a acquired AVM complicating a caesarean scar pregnancy, with successful outcome. The patient was a 38-year-old woman with two previous caesarean sections [5]. To date, we are not aware of any case in the international literature regarding the use of a liquid embolizing agent to treat twice a congenital AVM in a young girl. Due to our favourable immediate outcome, we believe that large studies should be performed to assess the safety, efficacy and long-term results of this particular way of treating conservatively congenital uterine AVMs.

There is no conflict of interest to declare.