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Case ReportpISSN 1738-2637 / eISSN 2288-2928J Korean Soc Radiol 2016;75(4):271-275http://dx.doi.org/10.3348/jksr.2016.75.4.271

Pancreatic arteriovenous malformation (AVM) is a rare condi-tion defined as a tumorous formation or vascular anomaly aris-ing from an aberrant bypass anastomosis of the arterial and ve-nous systems in the pancreas (1). Esophageal varix bleeding by portal venous hypertension is the most common complication of pancreatic AVM. Duodenal ulcer bleeding or bleeding from the pancreatic AVM itself are other causes of bleeding associated with this disease entity. Pancreatic AVM presenting as retroperi-toneal bleeding is an extremely rare clinical condition and is of-ten misdiagnosed as a pseudoaneurysm. Treatment may include ligation of the afferent artery, embolization of feeding vessels, portacaval shunting, or surgical resection of the affected part or the entire affected organ (2).

We report a case of pancreatic AVM presenting as a mesenteric hemorrhage that was successfully treated with transcatheter arte-rial embolization using n-butyl-2-cyanoacrylate (NBCA).

CASE REPORT

A 62-year-old man presented to the emergency department of our hospital with acute abdominal pain. He had no medical his-tory of alcohol abuse and no history of trauma. He experienced sudden-onset of severe periumbilical pain during defecation the morning on the day of admission. His vital signs were stable. Physical examination revealed mild periumbilical and rebound tenderness. Laboratory data showed a mild increase in white blood cell count (11600/µL) and increased lactate dehydrogenase level (938 IU/L). His hemoglobin, alanine aminotransferase, as-partate aminotransferase, amylase, and lipase levels were normal. A dynamic abdominal computed tomography (CT) scan showed diffuse hemorrhagic infiltration of the mesenteric root and peri-pancreatic area with compression of the superior mesenteric vein. In addition, a 1-cm nodular enhancing lesion was found

Transcatheter Arterial Embolization of Pancreatic Arteriovenous Malformation Presenting as Retroperitoneal Bleeding: A Case Report췌장 동정맥기형에 의한 후복막강 출혈: 사례 보고

Seung Woo Ji, MD1, Ung Rae Kang, MD1*, Young Hwan Kim, MD2

1Department of Radiology, Daegu Catholic Medical Center, Catholic University of Daegu College of Medicine, Daegu, Korea2Department of Radiology, Keimyung University College of Medicine, Keimyung University Dongsan Medical Center, Daegu, Korea

We report a case of pancreatic arteriovenous malformation presenting mesenteric and peripancreatic hemorrhages. A 62-year-old man presented to the emergency department of our hospital with acute periumbilical pain. Diffuse mesenteric and peripancreatic hemorrhages and an approximately 1 cm aneurysmal sac were ob-served on contrast-enhanced computed tomography. Celiac and superior mesenter-ic angiography revealed pancreatic arteriovenous malformation, which was then treated with transcatheter arterial embolization using n-butyl-2-cyanoacrylate. Complete obliteration of pancreatic arteriovenous malformation was evident on a follow-up computed tomography performed 2 months later.

Index termsArteriovenous MalformationPancreasHemorrhageTherapeutic Embolization

Received March 11, 2016Revised June 14, 2016Accepted August 17, 2016*Corresponding author: Ung Rae Kang, MDDepartment of Radiology, Daegu Catholic Medical Center, Catholic University of Daegu College of Medicine, 33 Duryugongwon-ro 17-gil, Nam-gu, Daegu 42472, Korea.Tel. 82-53-650-4328 Fax. 82-53-650-4339E-mail: urkang@cu.ac.kr

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distri-bution, and reproduction in any medium, provided the original work is properly cited.

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adjacent to the superior mesenteric artery (SMA) and dorsome-dial to the pancreatic head, which was prospectively diagnosed as a pseudoaneurysm of the mesenteric artery with mesenteric and peripancreatic hemorrhages (Fig. 1A). He was referred to the in-tervention department for further evaluation. Selective superior mesenteric arteriography revealed a nodular nidus at the pancre-atic head that was fed by a small branch of the inferior pancreati-coduodenal artery with a drainage vein to the upper superior mesenteric vein and early visualization of the portal vein (Fig. 1B, C). Another feeder of AVM was the dorsal pancreatic artery, branching from the proximal common hepatic artery just distal to the splenic artery bifurcation on celiac arteriogram (Fig. 1D, E). These findings were consistent with a pancreatic AVM. Owing to the relatively large extent of the hemorrhage and the presence of only two feeding arteries, endovascular treatment was considered to avoid invasive surgical excision. The feeding artery via the small branch of the inferior pancreaticoduodenal artery was easi-ly super selected with a 2.4-Fr microcatheter (Progreat, Terumo, Tokyo, Japan) through the SMA approach. However, the other feeding artery via the dorsal pancreatic artery was successfully catheterized retrogradely through the pancreaticoduodenal ar-cade, after a failed attempt through the celiac approach due to the very acute origin of the target artery. The feeding arteries were embolized with injection of NBCA (Histoacryl, B. Braun, Mel-sungen, Germany) diluted 1:4 (first artery) and 1:2 (second ar-tery) with iodized oil (Lipiodol, Guerbet, Aulnay-Sous-Bois, France). A post-procedure angiography revealed complete ex-clusion of the feeding arteries, nidus, and aberrant draining vein (Fig. 1F, G). The post-procedure course was uneventful, and the patient’s symptoms abated after the procedure. A follow-up CT scan obtained 2 months after the procedure showed complete disappearance of the pancreatic AVM and mesenteric hemor-rhage (Fig. 1H).

DISCUSSION

Pancreatic AVM is a rare condition defined as a tumorous for-mation or vascular anomaly arising from an aberrant bypass anastomosis of the arterial and venous systems in the pancreas (1). Halpern et al. (1) first reported a patient with pancreatic AVM associated with Rendu-Osler-Weber disease in 1968. Pan-creatic AVM is classified as a congenital anomaly thought to be

caused by failure of the regulatory sphincteric mechanism of the arteriole-capillary junction, resulting in unrestricted overflow of arterial blood into the capillary bed, or by acquired disease com-plicated by trauma, inflammation, or tumor.

Pancreatic AVM has various clinical manifestations, which may be asymptomatic or include abdominal pain, pancreatitis, and/or gastrointestinal (GI) bleeding. Nishiyama et al. (2) re-viewed the cases of 42 patients with pancreatic AVM. They re-ported that 50% of patients presented with life-threatening GI bleeding. The AVM was located in the pancreatic head in 56% of the patients, 31% of whom also had an extrapancreatic AVM (2). Makhoul et al. (3) classified the bleeding mechanisms of pancre-atic AVM into two categories as follows: first, bleeding from a ruptured esophageal or gastric varix secondary to portal hyper-tension induced by the AVM; and second, hemorrhage from di-rect erosion of the AVM into the pancreatic duct or through the adjacent intestinal mucosa as a duodenal ulcer. However, pancre-atic AVM presenting as retroperitoneal bleeding has been rarely documented. In the present case, the hemorrhage was present in the small bowel mesentery and peripancreatic retroperitoneal space. As the patient’s pain developed acutely during defecation, we assume that this rare instance of retroperitoneal bleeding was the result of an abrupt increase in portal venous pressure induced by increased intraperitoneal pressure.

Doppler ultrasonography is a non-invasive and easily repeated modality that can be performed at a patient’s bedside. Pancreatic AVM appears on Doppler ultrasonography as mosaic lesions composed of pulsatile waves, but ultrasonography has limitations in revealing the full extent of the lesion and its relation to adja-cent organs. The characteristic CT findings of AVM include nod-ular enhancement and early appearance of the portal venous sys-tem. Although nodular enhancement and early appearance of the portal venous system were observed in 76.9% and 66.7% of patients, respectively, in one study (4), some cases demonstrated uncharacteristic imaging findings that led to misdiagnosis as a pseudoaneurysm or a true aneurysm, as in the present case. Mag-netic resonance imaging (MRI) shows a tangle of tubular struc-tures with a signal void on T2-weighted image for high blood flow and hyperintense enhancement of tubular structures on en-hanced arterial phase, as a characteristic feature of AVM (5). However, MRI is not a widely used imaging modality for cases of acute bleeding. Dilated and tortuous feeding arteries, racemose

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staining in the nidus, and early appearance of the portal venous system have been reported as characteristic angiographic find-ings of AVM (4).

The treatment methods for pancreatic AVM are surgery (57.1%); nonsurgical therapy, including embolization, irradia-

tion, or a portovenous shunt (14.3%); and no treatment (28.6%) (2). Surgery is the least preferable treatment method because to-tal extirpation of the affected organ, or at least the involved por-tion, is the only way to assure a complete cure and eliminate the possibility of recurrent bleeding. However, excision of the pan-

Fig. 1. Transcatheter arterial embolization of pancreatic arteriovenous malformation in a 62-year-old man presenting as retroperitoneal bleeding.A. Portal-phase dynamic computed tomographic image shows an enhanced nodular vascular lesion with mesenteric and peripancreatic hemor-rhages adjacent to the pancreatic head (arrowheads). The superior mesenteric vein is compressed by hematoma (arrow).B. A selective superior mesenteric arteriogram shows a nodular nidus at the pancreatic head that is fed by a small branch of the inferior pancre-aticoduodenal artery (arrow).C. Delayed superior mesenteric arteriogram shows the tortuous drainage vein (arrowhead) to the superior mesenteric vein and early visualization of the portal vein (arrow).D. A selective celiac arteriogram shows a second feeding artery through the dorsal pancreatic artery that originates from the proximal common hepatic artery just distal to the splenic artery bifurcation (arrow).E. A selective dorsal pancreatic arteriogram through the pancreaticoduodenal arcade shows early visualization of the portal vein (arrow).F. A post-procedural angiogram shows complete exclusion of the feeding arteries, nidus, and aberrant draining vein.G. Indirect portogram after procedure shows patent portal venous flow despite spreading of several NBCA droplets in liver.H. A computed tomographic scan obtained 2 months after the procedure, shows complete embolization of the pancreatic arteriovenous malfor-mation and improved retroperitoneal hemorrhage.NBCA = n-buty1-2-cyanoacrylate

A

D

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C

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creatic head is a highly invasive procedure that carries a high risk of complications. Thus, the efficacy of surgery should be deter-mined after considering the size and location of the lesion. Sur-gery has also been reported to possibly have a limited value be-cause of inoperability or inaccessibility of the affected region (2). An endovascular approach is a good alternative for poor surgical candidates. Transarterial embolization (TAE) has been shown to be a good alternative treatment for the control of hemorrhage from various bleeding foci in cases of congenital AVM (6). Tasuta et al. (7) reported successful treatment of cases with TAE alone in patients without hemorrhagic complications. In their summary of 13 previous reports of pancreatic AVM treated with TAE, all patients with hemorrhagic complication initially treated with TAE required surgery. The recurrent bleeding rate after success-ful TAE has been reported to be up to 37% (7). Although com-plete regression of pancreatic AVM with numerous feeding arter-ies is difficult to achieve using TAE; complete embolization of the feeding arteries, nidus, and draining veins is achievable in pa-tients with a considerable number of feeding arteries. Successful treatment of pancreatic AVM using TAE with NBCA, or ethyl-ene vinyl alcohol copolymer (Onyx), has been reported (7, 8). Moreover, a transvenous approach has been reported to be a use-ful endovascular approach in patients with too many collateral arteries to embolize separately (6). However, transvenous embo-lization carries a high risk of increasing venous pressure, result-ing in catastrophic bleeding from the AVM. The commonly used embolic agents are metallic coil, gelatin sponge, and poly-vinyl-alcohol (PVA) particles. Metallic coil is an effective embolic agent, but it can embolize only the feeding artery, excluding the nidus and draining vein. Thus, the recurrence rate could be high through multiple other feeders. Furthermore, gelatin slurry and PVA particles carries the risk of migration of considerable amount of embolic agent to the distal vein via AVM, until complete oc-clusion is achieved. NBCA or Onyx is a commonly used perma-nent liquid embolic agent in TAE for AVMs in various other or-gans. NBCA and Onyx can achieve not only embolization of the feeding artery but also distal vasculature, including the nidus and draining vein. In the present case, only two feeding arteries to the pancreatic AVM were found on arteriography of the SMA and celiac artery. Super selection of the two feeders was successfully achieved using a microcatheter. For flow occlusion, we used a mixture of NBCA and iodized oil at ratios of 1:2 and 1:4 as a per-

manent embolization agent to delay polymerization for complete embolization of not only the feeding arteries but also the drain-ing veins. No considerable distal migration of NBCA to the por-tal vein was observed. Although low concentration of NBCA in-jection may result in reflux or distal migration of NBCA, which can lead to non-target embolization, a small amount of NBCA may not influence the main portal flow or liver function. The NBCA concentration should be adequately adjusted for its po-lymerization time to embolize the draining vein.

The present patient was followed up for only 2 months, but complete exclusion of the AVM with the disappearance of the ni-dus and the draining vein was observed on the follow-up CT scan.

In conclusion, we report a rare case of pancreatic AVM pre-senting as retroperitoneal bleeding, which was successfully treat-ed with TAE without any complications.

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2. Nishiyama R, Kawanishi Y, Mitsuhashi H, Kanai T, Ohba K,

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3. Makhoul F, Kaur P, Johnston TD, Jeon H, Gedaly R, Ranjan

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췌장 동정맥기형에 의한 후복막강 출혈: 사례 보고

지승우1 · 강웅래1* · 김영환2

급성 복통으로 내원한 62세 남자의 췌장 동정맥기형에 의한 출혈을 경동맥색전술로 치료한 증례에 대해 보고하고자 한다.

조영증강 전산화단층촬영에서 장간막과 췌장주위의 출혈과 함께 1 cm 크기의 동맥류성 낭이 발견되었다. 복강동맥과 위

창자간막 동맥 혈관조영술에서 췌장 동정맥기형이 발견되었고 n-butyl-2-cyanoacrylate를 사용하여 경동맥 색전술을 시

행하였다. 2개월 후 추적 전산화단층촬영에서 췌장 동정맥기형의 완전한 소실을 확인하였다.

1대구가톨릭대학교 의과대학 대구가톨릭대학교병원 영상의학과학교실, 2계명대학교 의과대학 동산의료원 영상의학과학교실