Digestive Diseases and Sciences, Vol. 37, No. 10 (October 1992), pp. 1619-1623
CASE REPORT
Arteriovenous Malformation of the Pancreas Associated with Hepatocellular Carcinoma A Case Report and Review of the Literature Y O S H I O M I U R A , MD, Y O S H I T A K A K A T O , MD, R O K U R O S E I K O , MD, M A R l N O M U R A , MD, K O S U K E Y A M A N E , MD, K O I C H I F U J I K A W A , MD, T O S H I Y U K I I W A M O T O , MD, and K I Y O H I K O D O H I , MD KEY WORDS: pancreatic AVM; liver cirrhosis; hepatocellular carcinoma.
Pancreatic arteriovenous malformation (AVM) with or without b o w e l lesions is a rare entity and is occasionally one of the manifestations of hereditary h e m o r r h a g i c telangiectasia ( O s l e r - W e b e r - R e n d u disease). Gastrointestinal bleeding is the m o s t frequent s y m p t o m but a s y m p t o m a t i c cases are found incidentally b y angiography. CASE REPORT
A 56-year-old Japanese man with chronic active hepatitis was admitted to our hospital for evaluation of hepatic tumors detected by ultrasonography and an elevated a-fetoprotein (a-FP) level. There were no specific complaints related to the gastrointestinal tract. On physical examination he had vascular spiders on the anterior chest but no other mucocutaneous lesions, and a hard liver could be palpated. Biochemical tests showed slight increases in asparate aminotransferase (104 units/liter, normal 14-36 units/liter), alanine aminotransferase (159 units/liter, normal 9-35 units/liter), leucine aminopeptidase (104 IU/liter, normal 27-50 IU/liter, and ~/-glutamyltranspeptidase (238 IU/liter, normal 14-65 IU/liter). Carcinoembryonic antigen was normal (1.4 ng/ml, normal less than 5 ng/ml) but a-FP was increased (123 ng/ml, normal less than 10 ng/ml). A serologic test for hepatitis B antigen was negative. Gastrin, glucagon, and vasointestinal peptide levels were within the normal range, but Manuscript received February 5, 1992; revised manuscript received April 24, 1992; accepted May 5, 1992. From the Departments of Surgery, Internal Medicine, Radiology, and Pathology, Hiroshima General Hospital of West Japan Railway Company; and 2nd Department of Surgery, Hiroshima University School of Medicine, Hiroshima, Japan. Address for reprint requests: Dr. Y. Miura, 2nd Department of Surgery, Hiroshima University School of Medicine, 1-2-3 Kasumi Minami-ku Hiroshima 734 Japan.
somatostatin was increased (143.7 pg/ml, normal 54 --- 4 pg/ml). Computed tomographic (CT) scan showed a lowdensity nodule in the right lower posterior segment ($6) of the liver. The pancreas appeared normal on plain and conventionally enhanced CT scan, but dilated feeding arteries and an intrapancreatic stain could be visualized after a bolus injection of contrast medium (Figure 1). Celiac arteriogram showed dilated feeding arteries, a racemose intrapancreatic vascular network, and early portal filling in the body of the pancreas (Figure 2). Hepatic arteriogram revealed a hypervascular stain in the right lobe of the fiver (Ss). Endoscopic retrograde pancreatogram (ERP) showed a normal pancreatic duct. Although the CT scan and angiographic findings were specific for pancreatic AVM, the rarity of pancreatic AVM and the hepatic deposits gave us the impression of a nonfunctional islet cell carcinoma with liver metastases. A distal pancreatectomy with splenectomy was performed on February 16, 1987. The pancreas appeared normal but the vascularity of the pancreatic capsule was increased. The hard consistency and irregular surface of the liver was consistent with cirrhosis. A thumb-sized nodule on the surface of the superior anterior hepatic segment ($8) was coagulated by microwave. Frozen sections of the resected pancreas and the hepatic tumor revealed no malignancy. Another tumor in $6, which had been detected by CT scan, could not be visualized by operative sonography. This tumor was left untreated as a distal pancreatectomy and simultaneous right hepatectomy seemed excessive for an unproven malignancy. Microscopically, the vascular lesion was located in the body of the pancreas and consisted of tortuous dilated vessels with thickened walls. Acinar tissue was partially atrophied and focally replaced by fibrosis which was consistent with mild chronic pancreatitis. The hepatic tumor was diagnosed as a hepatocellular carcinoma on permanent section.
Digestive Diseases and Sciences, Vol. 37, No. 10 (October 1992) 0163-2116/92/1000-1619506.50/0 9 1992 Plenum Publishing Corporation
1619
MIURA ET AL
Fig 1. (A) No abnormalities in the pancreas were seen on plain CT scan. (B) Dilated feeding arteries and an intrapancreatic hypervascular network could be observed in the body of the pancreas after a bolus injection of the contrast media. On cross section, the outline of the pancreas was normal despite hypervascularity.
1620
Digestive Diseases and Sciences, Vol. 37, No. 10 (October 1992)
PANCREATIC ARTERIOVENOUS MALFORMATION
Fig 2. Celiac arteriogram showed a hypervascular mass in the body of the pancreas, which was fed by dilated tortuous feeding arteries. The portal vein was already visualized at the same phase.
The postoperative course was uneventful. Transcatheter hepatic arterial embolizations were repeated until the patient died from hepatocellular carcinoma three and half years after the operation. DISCUSSION Pancreatic AVM is a rare entity. Fifteen cases, including our own, have been reported (Table 1) (1-12). Pancreatic AVM occurs solitarily or may be accompanied by other gastrointestinal lesions. There is no sexual predominance. Most of the patients are in the fifth and sixth decades. The most frequent symptom is gastrointestinal bleeding, and seven of the 15 cases had melena or hematemesis. Two cases had abdominal pain, one of these from duodenal ulcer compressed by the pancreatic mass. One case had cardiac failure due to increased arteriovenous shunting. Four cases, including our own, were asymptomatic and found incidentally. Gastrointestinal bleeding may occur by the following mechanisms: (1) rupture of the pancreatic AVM directly into pancreatic duct and subsequently into Digestive Diseases and Sciences, Vol. 37, No. 10 (October 1992)
the duodenum (9); (2) rupture of the accompanying intestinal AVMs (5); (3) bleeding from esophageal varices caused by increased portal hypertension (5); (4) erosion or ulcer of the duodenal wall compressed by the pancreatic AVM (2). Gastrointestinal AVM may be one of the manifestations of hereditary telangiectasia (OslerWeber-Rendu disease). Six of the 15 cases had Osler-Weber-Rendu disease, and none of those were Japanese. Angiography is the most definitive method of diagnosis. The characteristic features are as follows: (1) dilated and tortuous feeding arteries; (2) a racemose intrapancreatic vascular network and a transient dense stain; and (3) an early filling vein (5). Similar findings can be seen in acute or recurrent pancreatitis, but pancreatic AVM lacks the clinical picture of pancreatitis (13). Hypervascular pancreatic neoplasms like cystadenoma, cystadenocarcinoma, and islet cell tumor have to be taken into consideration for differential diagnosis, but those
1621
MIURA ET AL TABLE 1. PANCREATICARTERIOVENOUSMALFORMATION* Case age and sex (re t)
Symptom
33, F (1)
GI bleeding
52, M (2)
epigastric pain, easy fatigability GI bleeding, weakness
63, F (3) 7m, M (4, 5)
GI bleeding
68, F (4)
GI bleeding
63, F (5)
asymptomatic
56, M (5)
GI bleeding
35, F (6)
midepigastric pain
49, F (7)
cardiac failure
50, F (8)
massive epistasis, anemia GI bleeding GI bleeding
39, F (9) 52, M (10) 51, M (11) 53, M (12) 56, M (present case)
asymptomatic asymptomatic asymptomatic
Location o f A VM
body, tail of pancreas head of pancreas tail of pancreas, small and large bowel body of pancreas, duodenum, jejunum pancreas, liver, stomach, duodenum whole pancreas body, tail of pancreas whole pancreas, jejunum body of pancreas, uterus, pelvis, kidneys whole pancreas, jejunum body of pancreas pancreas, duodenum body of pancreas body of pancreas body, tail of pancreas
Treatment
Prognosis
OWR
+ pancreaticoduodenectomy
no bleeding for 5 months
resection of small and large bowel
+
partial duodenectomy, resection of jejunum
no bleeding for 14 months
synthetic estrogen (diethylstilbestrol)
no bleeding for 4 years
+
chemotherapy for rectal carcinoma distal pancreatectomy
alive for 6 months
-
dead 2 weeks after
+
celiac plexus block conservative therapy conservative therapy distal pancreatectomy 1)TAE, 2) pancreaticoduodenectomy, transverse colectomy conservative therapy conservative therapy distal pancreatectomy
+ alive for 15 months 1)duodenocolic fistula, 2) well after surgery
+
dead in 4.5 years (HCC)
-
*OWR: Osler-Weber-Rendu disease; GI bleeding: gastrointestinal bleeding; TAE: transcatheter arterial embolization; HCC: hepatocellular carcinoma.
tumor stains appear in the venous phase, and early venous filling is usually absent (5). In our case the angiographic findings were compatible with pancreatic AVM, but a well-demarcated hypervascular mass in the pancreas and a hepatic stain gave us the impression of a nonfunctional islet cell carcinoma with liver metastases. There appeared to be no abnormalities in the pancreas on plain CT scan. Bolus injection of contrast media revealed dilated feeding arteries, dense intrapancreatic stain that disappeared during the venous phase, and early portal filling. Despite the dense accumulation of contrast medium and clear demarcation of the lesion, the pancreatic outline on cross section was normal. Although angiography is essential for the diagnosis of pancreatic AVM, CT scan is also useful in following up a case in which surgical intervention is not possible. ERP was performed in three of the reported cases. Two of these were normal, but one case
1622
showed a normal main pancreatic duct with marked ascinar filling in the lesion without any evidence of chronic pancreatitis (1 I). Surgical extirpation of the affected organ is the proper treatment. Gastrointestinal bleeding from a pancreatic AVM may be lethal. Subtotal pancreatectomy or pancreaticoduodenectomy is indicated for uncontrollable bleeding. As AVMs gradually increase in size, and as extirpation of a pancreatic AVM was shown to improve portal hypertension (5), prophylactic distal pancreatectomy for AVM in the body or the tail of the pancreas may be justified. However, prophylactic pancreaticoduodenectomy or total pancreatectomy may be too excessive. If the lesion is throughout the entire pancreas, or the gastrointestinal tract is widely affected, transcatheter arterial embolization is another possible therapy, although complete regression is difficult and great care should be taken to prevent bowel necrosis (10). Digestive Diseases and Sciences, Vol. 37, No. 10 (October 1992)
PANCREATIC ARTERIOVENOUS MALFORMATION
SUMMARY A case of pancreatic arteriovenous malformation (AVM) with hepatocellular carcinoma is reported. The patient, a 56-year-old Japanese man, was asymptomatic. The pancreatic lesion was found incidentally during an evaluation for hepatocellular carcinoma. Celiac arteriogram demonstrated tortuous feeding arteries, a racemose intrapancreatic
6.
stain, which disappeared before the venous phase, and early portal filling.
9.
REFERENCES 1. Halpern M, Turner AF, Citron BP: Hereditary hemorrhagic teleangiectasia Radiology 90:1143-1149, 1968 2. Grannis FW, Foulk WT, Miller WE, Payne WS: Diagnosis and management of an arteriovenous fistula of pancreas and duodenum. Mayo Clin Pro 48:780-782, 1973 3. Lande A, Bedford A, Schechter LS: The spectrum of arteriographic findings in Osler-Weber-Rendu disease. Angiography 27:223-240, 1976 4. Moore JD, Thompso n NW, Appelman HD, Foley D: Arteriovenous malformations of the gastrointestinal tract. Arch Surg 111:381-389, 1976 5. Chuang VP, Pulmano CM, Walter JF, Cho KJ: Angiography
D~estive Diseases and Sciences, Vol. 37, No. 10 (October 1992)
7.
8.
10.
11.
12.
13.
of pancreatic arteriovenous malformation. Am J Roentgenol 129:1015-1018, 1977 Bdnley JL, Palubinskas AJ: Congenital arteriovenous malformation of the pancreas. Br J Radiol 50:219-222, 1977 Ishikawa T: Congenital arteriovenous malformations involving the pelvis and retrnperitoneum. Angiography 30:70-74, 1979 Lawhon NC: Radiologic seminar CCVI: Pancreatic arteriovenous malformation. J Miss State Med Assoc 2:184-185, 1980 Mizutani N, Masuda Y, Naito N, Toda T, Yao E, Fukumoto M: Pancreatic arteriovenous malformation in a patient with gastrointestinal hemorrhage. Am J Gastroenterol 76:141144, 1981 Gomes AS, Mali WP, Oppenheim WL: Embolization therapy in the management of congenital arteriovenous malformations. Radiology 144:41-49, 1982 Sawabu N, Ishida Y, Toya D, Yoneshima M, Hattori N, Kadoya M: Pancreatic arteriovenous malformation presenting as interesting findings on endoscopic retrograde pancreatography. Dig Dis Sci 29:678-682, 1984 Uchino A, Ishino Y, Ohno M: Arteriovenous malformation of the pancreas associated with mesenteric varices. Radiat Med 7:6-9, 1989 Roe M, Greenough WG: Marked hypervascularity and arteriovenous shunting in acute pancreatitis. Radiology 113:4748, 1974
1623
CASE REPORT
Arteriovenous Malformation of the Pancreas Associated with Hepatocellular Carcinoma A Case Report and Review of the Literature Y O S H I O M I U R A , MD, Y O S H I T A K A K A T O , MD, R O K U R O S E I K O , MD, M A R l N O M U R A , MD, K O S U K E Y A M A N E , MD, K O I C H I F U J I K A W A , MD, T O S H I Y U K I I W A M O T O , MD, and K I Y O H I K O D O H I , MD KEY WORDS: pancreatic AVM; liver cirrhosis; hepatocellular carcinoma.
Pancreatic arteriovenous malformation (AVM) with or without b o w e l lesions is a rare entity and is occasionally one of the manifestations of hereditary h e m o r r h a g i c telangiectasia ( O s l e r - W e b e r - R e n d u disease). Gastrointestinal bleeding is the m o s t frequent s y m p t o m but a s y m p t o m a t i c cases are found incidentally b y angiography. CASE REPORT
A 56-year-old Japanese man with chronic active hepatitis was admitted to our hospital for evaluation of hepatic tumors detected by ultrasonography and an elevated a-fetoprotein (a-FP) level. There were no specific complaints related to the gastrointestinal tract. On physical examination he had vascular spiders on the anterior chest but no other mucocutaneous lesions, and a hard liver could be palpated. Biochemical tests showed slight increases in asparate aminotransferase (104 units/liter, normal 14-36 units/liter), alanine aminotransferase (159 units/liter, normal 9-35 units/liter), leucine aminopeptidase (104 IU/liter, normal 27-50 IU/liter, and ~/-glutamyltranspeptidase (238 IU/liter, normal 14-65 IU/liter). Carcinoembryonic antigen was normal (1.4 ng/ml, normal less than 5 ng/ml) but a-FP was increased (123 ng/ml, normal less than 10 ng/ml). A serologic test for hepatitis B antigen was negative. Gastrin, glucagon, and vasointestinal peptide levels were within the normal range, but Manuscript received February 5, 1992; revised manuscript received April 24, 1992; accepted May 5, 1992. From the Departments of Surgery, Internal Medicine, Radiology, and Pathology, Hiroshima General Hospital of West Japan Railway Company; and 2nd Department of Surgery, Hiroshima University School of Medicine, Hiroshima, Japan. Address for reprint requests: Dr. Y. Miura, 2nd Department of Surgery, Hiroshima University School of Medicine, 1-2-3 Kasumi Minami-ku Hiroshima 734 Japan.
somatostatin was increased (143.7 pg/ml, normal 54 --- 4 pg/ml). Computed tomographic (CT) scan showed a lowdensity nodule in the right lower posterior segment ($6) of the liver. The pancreas appeared normal on plain and conventionally enhanced CT scan, but dilated feeding arteries and an intrapancreatic stain could be visualized after a bolus injection of contrast medium (Figure 1). Celiac arteriogram showed dilated feeding arteries, a racemose intrapancreatic vascular network, and early portal filling in the body of the pancreas (Figure 2). Hepatic arteriogram revealed a hypervascular stain in the right lobe of the fiver (Ss). Endoscopic retrograde pancreatogram (ERP) showed a normal pancreatic duct. Although the CT scan and angiographic findings were specific for pancreatic AVM, the rarity of pancreatic AVM and the hepatic deposits gave us the impression of a nonfunctional islet cell carcinoma with liver metastases. A distal pancreatectomy with splenectomy was performed on February 16, 1987. The pancreas appeared normal but the vascularity of the pancreatic capsule was increased. The hard consistency and irregular surface of the liver was consistent with cirrhosis. A thumb-sized nodule on the surface of the superior anterior hepatic segment ($8) was coagulated by microwave. Frozen sections of the resected pancreas and the hepatic tumor revealed no malignancy. Another tumor in $6, which had been detected by CT scan, could not be visualized by operative sonography. This tumor was left untreated as a distal pancreatectomy and simultaneous right hepatectomy seemed excessive for an unproven malignancy. Microscopically, the vascular lesion was located in the body of the pancreas and consisted of tortuous dilated vessels with thickened walls. Acinar tissue was partially atrophied and focally replaced by fibrosis which was consistent with mild chronic pancreatitis. The hepatic tumor was diagnosed as a hepatocellular carcinoma on permanent section.
Digestive Diseases and Sciences, Vol. 37, No. 10 (October 1992) 0163-2116/92/1000-1619506.50/0 9 1992 Plenum Publishing Corporation
1619
MIURA ET AL
Fig 1. (A) No abnormalities in the pancreas were seen on plain CT scan. (B) Dilated feeding arteries and an intrapancreatic hypervascular network could be observed in the body of the pancreas after a bolus injection of the contrast media. On cross section, the outline of the pancreas was normal despite hypervascularity.
1620
Digestive Diseases and Sciences, Vol. 37, No. 10 (October 1992)
PANCREATIC ARTERIOVENOUS MALFORMATION
Fig 2. Celiac arteriogram showed a hypervascular mass in the body of the pancreas, which was fed by dilated tortuous feeding arteries. The portal vein was already visualized at the same phase.
The postoperative course was uneventful. Transcatheter hepatic arterial embolizations were repeated until the patient died from hepatocellular carcinoma three and half years after the operation. DISCUSSION Pancreatic AVM is a rare entity. Fifteen cases, including our own, have been reported (Table 1) (1-12). Pancreatic AVM occurs solitarily or may be accompanied by other gastrointestinal lesions. There is no sexual predominance. Most of the patients are in the fifth and sixth decades. The most frequent symptom is gastrointestinal bleeding, and seven of the 15 cases had melena or hematemesis. Two cases had abdominal pain, one of these from duodenal ulcer compressed by the pancreatic mass. One case had cardiac failure due to increased arteriovenous shunting. Four cases, including our own, were asymptomatic and found incidentally. Gastrointestinal bleeding may occur by the following mechanisms: (1) rupture of the pancreatic AVM directly into pancreatic duct and subsequently into Digestive Diseases and Sciences, Vol. 37, No. 10 (October 1992)
the duodenum (9); (2) rupture of the accompanying intestinal AVMs (5); (3) bleeding from esophageal varices caused by increased portal hypertension (5); (4) erosion or ulcer of the duodenal wall compressed by the pancreatic AVM (2). Gastrointestinal AVM may be one of the manifestations of hereditary telangiectasia (OslerWeber-Rendu disease). Six of the 15 cases had Osler-Weber-Rendu disease, and none of those were Japanese. Angiography is the most definitive method of diagnosis. The characteristic features are as follows: (1) dilated and tortuous feeding arteries; (2) a racemose intrapancreatic vascular network and a transient dense stain; and (3) an early filling vein (5). Similar findings can be seen in acute or recurrent pancreatitis, but pancreatic AVM lacks the clinical picture of pancreatitis (13). Hypervascular pancreatic neoplasms like cystadenoma, cystadenocarcinoma, and islet cell tumor have to be taken into consideration for differential diagnosis, but those
1621
MIURA ET AL TABLE 1. PANCREATICARTERIOVENOUSMALFORMATION* Case age and sex (re t)
Symptom
33, F (1)
GI bleeding
52, M (2)
epigastric pain, easy fatigability GI bleeding, weakness
63, F (3) 7m, M (4, 5)
GI bleeding
68, F (4)
GI bleeding
63, F (5)
asymptomatic
56, M (5)
GI bleeding
35, F (6)
midepigastric pain
49, F (7)
cardiac failure
50, F (8)
massive epistasis, anemia GI bleeding GI bleeding
39, F (9) 52, M (10) 51, M (11) 53, M (12) 56, M (present case)
asymptomatic asymptomatic asymptomatic
Location o f A VM
body, tail of pancreas head of pancreas tail of pancreas, small and large bowel body of pancreas, duodenum, jejunum pancreas, liver, stomach, duodenum whole pancreas body, tail of pancreas whole pancreas, jejunum body of pancreas, uterus, pelvis, kidneys whole pancreas, jejunum body of pancreas pancreas, duodenum body of pancreas body of pancreas body, tail of pancreas
Treatment
Prognosis
OWR
+ pancreaticoduodenectomy
no bleeding for 5 months
resection of small and large bowel
+
partial duodenectomy, resection of jejunum
no bleeding for 14 months
synthetic estrogen (diethylstilbestrol)
no bleeding for 4 years
+
chemotherapy for rectal carcinoma distal pancreatectomy
alive for 6 months
-
dead 2 weeks after
+
celiac plexus block conservative therapy conservative therapy distal pancreatectomy 1)TAE, 2) pancreaticoduodenectomy, transverse colectomy conservative therapy conservative therapy distal pancreatectomy
+ alive for 15 months 1)duodenocolic fistula, 2) well after surgery
+
dead in 4.5 years (HCC)
-
*OWR: Osler-Weber-Rendu disease; GI bleeding: gastrointestinal bleeding; TAE: transcatheter arterial embolization; HCC: hepatocellular carcinoma.
tumor stains appear in the venous phase, and early venous filling is usually absent (5). In our case the angiographic findings were compatible with pancreatic AVM, but a well-demarcated hypervascular mass in the pancreas and a hepatic stain gave us the impression of a nonfunctional islet cell carcinoma with liver metastases. There appeared to be no abnormalities in the pancreas on plain CT scan. Bolus injection of contrast media revealed dilated feeding arteries, dense intrapancreatic stain that disappeared during the venous phase, and early portal filling. Despite the dense accumulation of contrast medium and clear demarcation of the lesion, the pancreatic outline on cross section was normal. Although angiography is essential for the diagnosis of pancreatic AVM, CT scan is also useful in following up a case in which surgical intervention is not possible. ERP was performed in three of the reported cases. Two of these were normal, but one case
1622
showed a normal main pancreatic duct with marked ascinar filling in the lesion without any evidence of chronic pancreatitis (1 I). Surgical extirpation of the affected organ is the proper treatment. Gastrointestinal bleeding from a pancreatic AVM may be lethal. Subtotal pancreatectomy or pancreaticoduodenectomy is indicated for uncontrollable bleeding. As AVMs gradually increase in size, and as extirpation of a pancreatic AVM was shown to improve portal hypertension (5), prophylactic distal pancreatectomy for AVM in the body or the tail of the pancreas may be justified. However, prophylactic pancreaticoduodenectomy or total pancreatectomy may be too excessive. If the lesion is throughout the entire pancreas, or the gastrointestinal tract is widely affected, transcatheter arterial embolization is another possible therapy, although complete regression is difficult and great care should be taken to prevent bowel necrosis (10). Digestive Diseases and Sciences, Vol. 37, No. 10 (October 1992)
PANCREATIC ARTERIOVENOUS MALFORMATION
SUMMARY A case of pancreatic arteriovenous malformation (AVM) with hepatocellular carcinoma is reported. The patient, a 56-year-old Japanese man, was asymptomatic. The pancreatic lesion was found incidentally during an evaluation for hepatocellular carcinoma. Celiac arteriogram demonstrated tortuous feeding arteries, a racemose intrapancreatic
6.
stain, which disappeared before the venous phase, and early portal filling.
9.
REFERENCES 1. Halpern M, Turner AF, Citron BP: Hereditary hemorrhagic teleangiectasia Radiology 90:1143-1149, 1968 2. Grannis FW, Foulk WT, Miller WE, Payne WS: Diagnosis and management of an arteriovenous fistula of pancreas and duodenum. Mayo Clin Pro 48:780-782, 1973 3. Lande A, Bedford A, Schechter LS: The spectrum of arteriographic findings in Osler-Weber-Rendu disease. Angiography 27:223-240, 1976 4. Moore JD, Thompso n NW, Appelman HD, Foley D: Arteriovenous malformations of the gastrointestinal tract. Arch Surg 111:381-389, 1976 5. Chuang VP, Pulmano CM, Walter JF, Cho KJ: Angiography
D~estive Diseases and Sciences, Vol. 37, No. 10 (October 1992)
7.
8.
10.
11.
12.
13.
of pancreatic arteriovenous malformation. Am J Roentgenol 129:1015-1018, 1977 Bdnley JL, Palubinskas AJ: Congenital arteriovenous malformation of the pancreas. Br J Radiol 50:219-222, 1977 Ishikawa T: Congenital arteriovenous malformations involving the pelvis and retrnperitoneum. Angiography 30:70-74, 1979 Lawhon NC: Radiologic seminar CCVI: Pancreatic arteriovenous malformation. J Miss State Med Assoc 2:184-185, 1980 Mizutani N, Masuda Y, Naito N, Toda T, Yao E, Fukumoto M: Pancreatic arteriovenous malformation in a patient with gastrointestinal hemorrhage. Am J Gastroenterol 76:141144, 1981 Gomes AS, Mali WP, Oppenheim WL: Embolization therapy in the management of congenital arteriovenous malformations. Radiology 144:41-49, 1982 Sawabu N, Ishida Y, Toya D, Yoneshima M, Hattori N, Kadoya M: Pancreatic arteriovenous malformation presenting as interesting findings on endoscopic retrograde pancreatography. Dig Dis Sci 29:678-682, 1984 Uchino A, Ishino Y, Ohno M: Arteriovenous malformation of the pancreas associated with mesenteric varices. Radiat Med 7:6-9, 1989 Roe M, Greenough WG: Marked hypervascularity and arteriovenous shunting in acute pancreatitis. Radiology 113:4748, 1974
1623
