A 22-year-old male with a history of hypertension, obesity, and prior renal transplant presented to our institution with gunshot injuries to his abdomen. He underwent multiple open surgical procedures to remove the shrapnel and treat visceral organ injuries. His hospital course was complicated by renal failure requiring hemodialysis, severe intra-abdominal adhesions resulting in a frozen abdomen, persistent intra-abdominal infections and recurrent enteroatmospheric fistulae despite surgical revisions and loss of abdominal fascia preventing abdominal wound closure. These were treated using total parental nutrition and complex and intensive wound care using an ostomy apparatus and abdominal wound vac. Several months into his hospital course, he was noted to have blood within the ostomy bag and a persistent decrease in his hematocrit. The patient underwent endoscopy and additional exploratory surgery, but no clear source of bleeding was found. The patient had persistent bleeding that was minimally responsive to blood transfusions.

A contrast enhanced CT scan demonstrated fistulous connections between the hepatic arterial system and the portal venous system, a new finding from prior scans (Figure 1). A hepatic arteriogram demonstrated two large high flow arterio-portal fistulae supplied by the right hepatic artery (Figure 2). After selective catheterization of the feeding arteries with a microcatheter (Progreat, Terumo Tokyo, Japan), multiple detachable microcoils (Axiom, EV3 Irvine, USA) were deployed to completely occlude the arteriovenous communications. A post-embolization angiogram revealed successful occlusion of the treated fistulae but persistent arterio-portal shunting through multiple, but previously unidentified, small arteries feeding the portal vein through multiple small fistulous communications (Figure 3). Given the presence of multiple fistulous small communications, we decided to treat it like an arteriovenous malformation.

Figure 1: Coronal MPR CECT demonstrating opacification of the portal vein consistent with a large right arterioportal fistula.

Figure 2: DSA celiac angiogram redemonstrating large right-sided arterioportal fistula.

Figure 3: Post coil embolization DSA celiac angiogram-persistent filling of the fistula through small nidi.

Two weeks later, the patient returned to the angiography suite. Repeat celiac angiogram confirmed the previously identified findings of persistent arterio-portal communications from multiple small arterioles (Figure 4). A microcatheter (Progreat, Terumo, Tokyo, Japan) was advanced through the feeding vessels as close to the arterioportal communications as possible and embolization was performed with n-butyl cyanoacrylate (n-BCA), mixed with iodized oil (Lipiodol; Guerbet, Aulnay-sous-Bois, France) at a ratio of 1:4. A total of 5.5 mL of nBCA-iodized oil was injected. At the end of the procedure, there was significant reduction of flow through the fistulae and minimal opacification of the portal vein. Clinically, the patient’s bleeding decreased, but he remained transfusion dependent.

Figure 4: DSA arterial angiogram post coiling demonstrates with nidus (white arrow) and associated portal vein filling.

After four weeks, the patient was brought back to the angiographic suite for a repeat procedure. The celiac axis angiogram re-demonstrated multiple small feeding arteries feeding the right hepatic arterioportal communications outside of those treated previously. These branches predominantly arose from the cystic artery and the portions of the right hepatic artery supplying segments 7 and 8. Each of these arteries was selected with a microcatheter and embolized using nBCA mixed with lipiodol at a ratio of 1:4. A total of 6 mL of nBCA-lipiodol solution was used. A post-embolization angiogram demonstrated minimal persistent arterioportal shunting (Figure 5).

Figure 5: DSA post 2^nd nBCA glue embolization showing near complete obliteration of the shunt with minimal portal vein opacification.

After the embolization, the patient’s bleeding decreased. Four months after the last embolization procedure, the patient continued to experience wound bleeding requiring transfusion. Surgical closure of the open wounds was planned. Interventional radiology was consulted to evaluate for a recurrent arterioportal communication as a potential cause of bleeding and to consider portal decompression via a TIPS shunt placement to reduce surgical blood loss. Hemodynamic evaluation through free and wedged hepatic venous pressure measurements revealed a normal portosystemic gradient. A celiac angiogram revealed complete occlusion of all the fistulous communications without portal vein opacification (portal vein was patent on portal venous phase of the celiac arteriogram) (Figure 6).

Figure 6: DSA celiac angiogram showing complete obliteration of the shunt post nBCA glue placement.

The patient underwent successful primary wound closure with minimal blood loss. There were no delayed sequelae of arterioportal fistulae, such as portal hypertension, bowel edema, or hepatic failure. He is currently undergoing continued abdominal wound care with plans for skin grafting in the future.

Arterioportal fistulae and malformations are uncommon entities [1]. Most often, intrahepatic arterioportal fistulae occur secondary to direct liver trauma or with malignancy [2-8]. Associated complications include portal hypertension, distal embolization (pulmonary), and congestive heart failure [1,9]. A second etiology of arterioportal fistulae in pediatric populations is arterioportal fistula syndrome, a congenital disorder where multiple arterioportal fistulae develop in the absence of other arteriovenous abnormalities [3]. Arterioportal malformations are rare and most often are congenital in nature [10,11]. The limited literature suggests that these occur in isolation, with a possible association to conditions resulting in malformations in other locations such as hemorrhagic hereditary telegantecasia [12]. Regardless of etiology, similar complications result from both arteriportal fistulae and malformations.

Due to multiple life threatening associated complications, timely and effective treatment of arteriovenous fistulae/malformations is critical. Approaches to treatment have included both surgical and endovascular techniques. Endovascular treatments are preferred due to the rich vascular supply of the liver and the relative ease of treatment using this approach [1-3,5,13]. Most prior described endovascular therapies for these AV fistulas have described a coil-based approach [2,3,6,9,13-19]. This has also been the primary approach employed to treat vascular fistulas at other sites [20-22].

Arteriovenous malformations require a different form of treatment. The key differentiating factor between an arteriovenous malformation and fistula is the number of source arteries and the presence of a nidus. Fistulas have one or two relatively large feeding vessels that feed the shunt. Malformations are characterized by multiple smaller feeding vessels [23] which communicate with single/multiple draining veins through a nidus. While a fistula can easily be treated with coils deployed in the feeding artery, the mainstay for endovascular treatment of malformations is obliterating the nidus using liquid embolic materials such as ethylene vinyl alcohol copolymer (Onyx, Coviden, EV3, Plymouth, MN) or nBCA [24-27]. In fistulae, embolization with nBCA is used as a secondary technique, only if initial coil embolization is unsuccessful or fails. nBCA is avoided in many AV fistulae due to the difficulty in optimal positioning of the embolic material and the high risk of distal embolization [28]. In our literature search, we found only two cases where nBCA was used as the primary embolization method for post traumatic arteriorvenous fistulae, [29-31]. nBCA has been successfully employed in embolization of arteriovenous malformations in multiple other sites including the central nervous system, lungs, and extremities[32-34]. Limited data exists on treatment of arteriovenous malformations in the liver, and most interventions have occurred in pediatric populations [35,36].

In our patient, coil embolization was attempted initially as he had large documented arterioportal fistulae. Post coiling, multiple feeding vessels from the right hepatic arterial system, which were not seen initially, continued to shunt through multiple small fistulous communications. For effective disruption of these communications, the majority or all of these communications would have to be occluded. Embolizing the right hepatic arterial system can result in multiple biliary complications including gallbladder infarction and intrahepatic biliary occlusion [37]. This is particularly a concern in transplant livers but can occur in healthy non-transplant livers as well. Limited reports have demonstrated the effective use of nBCA for embolotherapy of acute hepatic arterial hemorrhage in healthy livers [4,38,39] and for treatment of arterioportal fistula [9,30,31]. As such, nBCA was felt to be a safer alternative, as it could be targeted primarily to the multiple small fistulous communications while maintaining relative hepatic artery patency.

The uniqueness of this case is that the patient developed complex small fistulous communications following embolization of large arterioportal fistulae. Though it is possible that these communications existed prior to embolization of large fistulae but were masked by high flow through the large fistulae, it is of authors’ opinion that these small fistulous communications developed through collateralization of distal segments of the occluded hepatic artery branches. Such intrahepatic arterial collateralization is well known following embolization of hepatic arterial branches during planning of intra-arterial Yttrium-90 microsphere therapy (reference needed).

Portal hypertension is a relatively common complication of arterioportal fistula and can result in the development of varices, bowel edema, and hepatic failure. Most reports suggest treating the underlying cause before addressing the portal hypertension with a decompressive treatment such as TIPS [1,9]. As the patient had recurrence of bleeding post embolization, he was assessed for presence of portal hypertension. On repeat angiogram, no evidence of portal hypertension was found and shunt obliteration was confirmed. We postulate that the residual arterio-portal shunting that persisted after the 2nd embolization eventually got occluded without any additional therapy secondary to slow flow in these fistulous communications. This delayed occlusion has been demonstrated following embolization of vascular malformations in other locations (particularly intracranial) [40-44].

In the present case report, we report the use of nBCA in the treatment of an acquired complex arterioportal fistula. This fistula was of traumatic etiology and resulted in ongoing hemodynamically significant bleeding. Initially, coil embolization was used to treat the large feeding arteries of a presumed simple AV fistula, but subsequent discovery of multiple small feeding arteries led an attempt of closure with a liquid embolic material that allowed successful occlusion with preserved parenchymal perfusion. The procedure was well tolerated without any complications or distal embolization.