Rare Cause of Gastrointestinal Bleeding: A Case Report of Pancreatic Arteriovenous Malformation

Background

Gastrointestinal arteriovenous malformation (AVM) is an unusual cause of gastrointestinal bleeding, accounting for less than 5% of cases of nonvariceal upper gastrointestinal bleeding [1]. AVM is characterized by an abnormal network of vessels that connect directly between a supplying artery and a draining vein, without intervening capillaries. The manifestations of pancreatic AVMs range from asymptomatic cases to cases of abdominal pain, gastrointestinal bleeding, and hypovolemic shock [2]. Therefore, it is challenging to diagnose pancreatic AVM by endoscopy or clinical examination, and imaging evaluation is needed to make a definitive diagnosis. Conventional treatment for AVMs of the gastrointestinal tract is surgical intervention; however, transcatheter arterial embolization (TAE) also is useful in selected cases [3]. Herein, we report the case of a 37-year-old man who presented with abdominal pain and gastrointestinal bleeding due to a pancreatic AVM, which was successfully treated with pancreaticoduodenectomy. We also present a review of the associated literature.

Case Report

A 37-year-old man with underlying hypertension and no significant family history was admitted to our hospital with a 3-month history of intermittent epigastric pain radiating to the back and unintentional weight loss of 5 kg in 2 months. He denied any antiplatelet or anticoagulant use prior to presentation. He was treated with an empiric proton pump inhibitor, which did not relieve his pain. At the initial evaluation, he had normal vital signs, and physical examination showed a mild tenderness in the epigastric region, without a palpable mass or bruit. The laboratory test results revealed a white blood cell count of 9.92 G/L with 68% neutrophils, moderate anemia, with a hemoglobin level of 8.9 g/dL and a red blood count of 4.09 G/L, platelet count of 427 G/L, glucose level of 4.72 mmol/L, normal serum level of lipase of 7.1 U/L, amylase level of 2.8 U/L, sodium level of 137 mmol/L, potassium level of 4.0 mmol/L, aspartate transaminase level of 17 U/L, alanine transaminase level of 15 U/L, total bilirubin level of 7 umol/L, urea level of 4.62 mmol/L, and creatinine level of 0.72 mg/dL.

The esophagogastroduodenoscopy revealed a large ulcer of 2 to 3 cm on the posterior wall of the second part of the duodenum, which was covered with pseudomembranous, little black blood at the bottom of the ulcer (Figure 1). With a large duodenal ulcer not controlled with a proton pump inhibitor, an abdominal computed tomography (CT) scan with contrast was indicated on day 3 and revealed an enhanced mass of 2.5×3.5×4 cm in size, located on the second and third parts of the duodenum and in the head of the pancreas, with no clear border and no washout effect on the arterial, venous, and late phases.

Angio-CT findings suggested that the feeder’s vessel was the superior mesenteric artery, and the outflow vessel drained into the portal vein and superior mesenteric vein, which suggested an AVM, differing from neuroendocrine neoplasms (Figure 2). The serum gastrin level was mildly elevated at 263 pg/mL (reference range 0–100 pg/mL). On day 7, abdominal magnetic resonance imaging was done to explore the gastrin-secreting tumor and revealed heterogeneous parenchyma of the head and isthmus of the pancreas, increasing signal on T2-weighted imaging, coil-like shape after administering contrast, and spreading to the second part of the duodenum (Figure 3). The patient was initially treated with proton pump inhibitors and pain killers, which provided modest relief in alleviating the patient’s pain, without new symptom onset in the subsequent days.

On day 10 of admission, the patient suddenly had sharp epi-gastric pain and melena. Vital signs included a heart rate of 120 beats per min, blood pressure of 100/60 mmHg, and hemoglobin level of 5.6 g/dL. He was resuscitated with fluid and blood transfusion. Because the urgent upper endoscopy did not control the acute hemorrhage, an angiography intervention was indicated (Figure 4). After angiographic embolization, the patient was stable, the melena stopped, the pain was relieved, and his hemoglobin level was 10.5 g/dL. The patient was discharged 5 days later, with no new symptoms.

Two weeks later, the patient suddenly had an episode of epi-gastric pain and he was re-admitted due to melena. His vital signs were within normal limits. Laboratory test results revealed his hemoglobin level decreased to 5 g/dL. The Whipple procedure was performed to prevent future bleeding. The pathology report showed there were many dilated, thin-walled veins and arteries in the pancreatic head (Figure 5). The patient was stable after the operation and was discharged after 18 days of hospitalization. At the 1-year follow-up, the patient was in good condition, and there had been no further episodes of gastrointestinal bleeding. The flowchart shown in Figure 6 describes all events of the patient’s case.

Discussion

Gastrointestinal AVM is an uncommon cause of gastrointestinal bleeding, which accounts for less than 5% of nonvariceal upper gastrointestinal bleeding [1]. AVM is characterized by vascular abnormalities, which are the direct connection of arteries and veins. Song et al reported that the median age of patients with AVM was 50 years, ranging from 7 months to 75 years, with an Asian (78.3%) and male (88.4%) predominance [4]. The clinical manifestation includes asymptomatic cases to cases with hemorrhagic shock conditions. The most common symptoms were gastrointestinal bleeding (49.3%) and abdominal pain (40.6%), and 18.8% of cases were asymptomatic [5]. AVM of the gastrointestinal tract is found most often in the cecum and the right side of the colon; however, duodenal AVM is rare and accounts for 2.3% of all AVMs of the gastrointestinal tract. Pancreatic AVM is most likely presented with hemorrhage in the head of the pancreas, whereas pancreatitis often occurs in the tail [6]. Portal hypertension or liver cirrhosis will eventual develop in 11% of patients [7].

The causes of pancreatic AVM consist of congenital or acquired etiologies. The main cause of pancreatic AVM is congenital in origin, accounting for approximately 90% of cases of pancreatic AVM, including Osler-Weber-Rendu disease. Other causes consist of trauma, pancreatitis, and tumors [8]. Our case was likely congenital in origin because the patient was young and had no history of pancreatitis, tumor, or trauma. Tsuyoshi et al suggested 4 mechanisms of pancreatic AVM-induced bleeding: (1) abnormal vessels of pancreatic AVM cause the infarction of the duodenal mucosa, leading to duodenal ulcer and gastrointestinal bleeding; (2) bleeding from the pancreatic duct and/or the bile duct; (3) bleeding due to vessels of pancreatic AVMs protruding on the lumen of the duodenum; and (4) variceal gastrointestinal bleeding due to portal hypertension [5]. In our case, there was a large duodenal ulcer without gastrointestinal varies and other bleeding sites found by endoscopy, no abnormalities in the bile duct and pancreatic duct detected by imaging findings, and no obvious bleeding sites in surgery. Therefore, it was likely that the bleeding origin of this patient was a duodenal ulcer caused by pancreatic AVM.

Gastrointestinal AVMs can be missed owing to the nonspecific symptoms and very low incidence of this entity. Therefore, it is essential to add AVM to the list of differential diagnoses, especially for patients who are not responsive to medical therapy. Our case is unique because the patient presented with abdominal pain, weight loss, and a large duodenal ulcer without signs of acute gastrointestinal bleeding on endoscopy. Doctors should question whether gastrointestinal ulcers not improving with proton pump inhibitors may have other causes. This patient also had a differential diagnosis of Zollinger-Ellison syndrome, which presented with a refractory duodenal ulcer and elevated gastrin level. However, it was not compatible with findings on abdominal magnetic resonance imaging and the pathology report, which made gastrinoma less likely in this patient.

Imaging modalities play an important role in the diagnosis of AVMs. Doppler ultrasonography can demonstrate mosaic lesions, including pulsatile waves in typical cases [9].

Three-dimensional imaging reconstructed using CT is commonly indicated and demonstrates the network of multiple intrapancreatic and peripancreatic vessels with early enhancement of the portal vein in the arterial phase [10]. Angiography is the definitive diagnostic modality for pancreatic AVM, with the findings typical for features including dilated and tortuous feeding arteries, a racemose intrapancreatic vascular network, and early filling veins, followed by early clearance of the pancreatic stain [11].

Surgical resection is the mainstay treatment modality of pancreatic AVM, particularly in symptomatic patients without portal hypertension [6]. The surgery resolves the cause of bleeding, which prevents the development of portal hypertension [5]. TAE, transjugular intrahepatic portosystemic shunt, and radio-therapy can be alternative approaches for patients with portal hypertension or for those at high risk for surgery [12,13]. Some authors suggest that preoperative TAE can reduce the blood flow to the portal system and the risk of recurrent bleeding after surgery. There are cases successfully treated with TAE alone, particularly in patients without hemorrhage [3,5]. Furthermore, TAE can be the temporary modality to control bleeding before undergoing more definitive therapy [3,14]. However, recurrent bleeding after TAE has been reported in up to 18% to 37% of patients waiting for surgery [5]. The main reason for the failure of TAE is that the multiple malformed blood vessels cannot be completely embolized; in addition, new collateral circulations between these vessels result in recurrence [4,11]. It is also important to consider complications of embolization, such as bowel ischemia [15]. Therefore, TAE can be considered in patients with a single feeder artery or no hemorrhage, or who are at high risk of surgery. Our case was initially successful with TAE to control the acute gastrointestinal bleeding; however, the patient had bleeding recur 4 weeks later since the AVM was supplied by multiple vessels. Therefore, surgical intervention was deemed appropriate for this patient.

Conclusions

In summary, pancreatic AVMs are rare but should be listed on the differential diagnosis in patients with abdominal pain and/or upper gastrointestinal bleeding, particularly those with non-healing and large duodenal ulcers. Early imaging modalities in patients with uncertain etiologies of gastrointestinal bleeding should be considered, and angiography is the most useful method for the diagnosis of pancreatic AVMs. Although surgical intervention is still the mainstay treatment, TAE could be indicated in specific conditions, particularly as a bridging and temporary method to control acute bleeding before the definitive therapy.