Congenital Hepatic Arterioportal Fistula in a 3-Year-Old Child

Abstract

Intrahepatic arterioportal fistula (APF) is a rare cause of portal hypertension. Although it may be congenital or acquired, most often it develops after trauma or iatrogenically after transhepatic interventions. Spontaneous APF may develop in patients with hepatocellular carcinoma or rupture of a hepatic artery aneurysm. Congenital lesions are rare. Isolated congenital APFs may have initial symptoms of portal hypertension, failure to thrive, diarrhea, and malabsorption. To date, all reported pediatric patients have had symptoms develop in the first year of life (1-10). We report the case of a 3-year-old patient with a congenital APF. CASE REPORT A 3-year-old boy had a 1-month history of weight loss and diarrhea and a 2-week history of fever. Initial blood, urine, and stool cultures were negative. Despite empirical treatment with amoxicillin, the fever persisted. Abdominal distension prompted an abdominal ultrasound, which revealed a vascular mass within the liver and mild splenomegaly. Abdominal computed tomographic scan suggested a mass originating from the adrenal gland. He was transferred to our institution with a provisional diagnosis of neuroblastoma. Medical history showed an unremarkable pregnancy and delivery. Birth weight was 3.3 kg. There was no history of trauma or surgery. the patient was admitted to a hospital for pneumonia at 3 months and 27 months of age. Results of a sweat test were positive but a second one and subsequent genetic testing for cystic fibrosis produced negative results. There was no history of hematemesis, rectal bleeding, or melena. During the month before admission, his stools were looser than usual, and his body weight decreased by approximately 2 kg. On physical examination, weight was 13.27 kg (25th percentile) and height 95.2 cm (50th percentile). Heart rate was 86 beats per minute, blood pressure was 104/56, respiratory rate was 24, and he was afebrile. Abdominal distension was noted. The liver was 3 cm below the right costal margin, and a continuous murmur was heard over the liver. The spleen was not palpable. Findings in cardiopulmonary examination were within normal limits. Laboratory results were: white blood cell count 4.5 × 103/mm3, hemoglobin 8.0 g/dl, and platelet count 547 × 103/mm3. Prothrombin and partial thromboplastin times were normal, and serum electrolytes, liver enzymes, and bilirubin were at normal levels. Serum proteins were 6.3 g/dl, and serum albumin was 3.4 g/dl. Abdominal ultrasound showed mild splenomegaly with an enlarged hepatic artery feeding a hypoechoic vascular liver lesion. The portal vein was enlarged and pulsatile with hepatofugal flow. Echocardiography showed a large patent ductus arteriosus (PDA), a small apical muscular ventricular septal defect, and left auricular and ventricular enlargement. The right ventricle was normal. Cardiac function was described as good. The patient was discharged home, and iron supplements were prescribed. He returned 6 weeks later for cardiac catheterization to occlude the PDA. He had lost 1.9 kg and had poor oral intake and markedly decreased activity. His resting heart rate was 160. He had cachexia and was dehydrated. After rehydration, hemoglobin was 6.6 g/dl, albumin was 2.8 g/dl, and prealbumin 13.6 mg/dl. An abdominal radiograph showed multiple dilated loops of bowel and air-fluid levels. After transfusion, he underwent cardiac catheterization. A small PDA was embolized. There was a small apical restrictive muscular ventricular septal defect. A diagnosis of large hepatic APF was made. The fistula was caused by a direct communication between a branch of the right hepatic artery and a venous structure with a large dilated aneurysm traversing toward the left branch of the portal vein and opening close to the entrance of the umbilical vein into the left portal branch. There was therefore a communication between the artery and the anomalous venous structure and communication of this structure with the left portal branch, similar to a long venous tract. The hepatic artery was enlarged, and there was hepatofugal flow in the portal vein (Figs. 1A, 1B, 1C). The portal vein was enlarged. The catheter was placed in the hepatic artery, then through the fistula into the portal vein, and a pressure of 30 mmHg was obtained in the portal vein. The cardiologist attempted an embolization of the APF with two 12-mm × 8-cm 0.038 Gianturco coils (Wilson-Cook Medical, Inc., Winston-Salem, NC, U.S.A.).FIG. 1: (A) Image from an abdominal aortogram, frontal projection, obtained during cardiac catheterization. Arterial phase showing an enlarged hepatic artery communicating with the portal venous system through a large arterioportal fistula. Arrow indicates the rent of the fistula. Arrowheads indicate direction of the flow. (B) Venous phase showing filling of the portal system from the fistula. Arrowheads indicate direction of flow. (C) Late venous phase showing filling of the splenic vein and the superior mesenteric vein. Arrowheads indicate direction of flow.Two days later, the patient returned to the cardiac catheterization laboratory to undergo embolization of the remainder of the APF. The fistula was still patent, and the flow in the portal vein was hepatofugal. Portal pressure was 34 mmHg. Occlusion of the APF at the communication between the long venous tract and the left portal branch, away from the fistulous rent, was mistakenly performed with nine 12-mm × 8-cm 0.038 Gianturco coils. A small branch of the portal vein in the right posterolateral lobe was also occluded with three 3-mm × 2-cm 0.038 Gianturco coils. The embolization was thought to be adequate, but a Doppler study the next day showed persistent hepatofugal pulsatile flow in the portal vein and a markedly enlarged hepatic artery feeding the APF. Despite these findings, he was sent home. The patient's nutritional status deteriorated, and he was admitted 2 weeks later to a peripheral hospital for institution of nasogastric feedings. Emesis soon developed and became bloody, with melena. He was transferred to our center. On admission, his weight was 12 kg. He had tachycardia, cachexia, and mild dehydration. The liver was palpated at 2 cm below the right costal margin with no thrill or bruit. The spleen was not palpable. Gastric lavage produced coffee ground-like material. Laboratory values were white blood cell count 18.6 × 103/mm3, hemoglobin 9.9 g/dl, platelet count 611 × 103/mm3, normal prothrombin and partial thromboplastin times, serum sodium 120 mmol/l, potassium 6.2 mmol/l, chloride 80 mmol/l, CO2 22 mmol/l, urea 26 mg/dl, creatinine 0.5 mg/dl, aspartate aminotransferase 105 U/l, alanine aminotransferase 65 U/l, alkaline phosphatase 248 U/l, γ-glutamyl transferase 167 U/l, total bilirubin 0.8 mg/dl, serum proteins 7.9 g/dl, and albumin 4.6 g/dl. An abdominal radiograph was within normal limits, except for the metal coils. Abdominal ultrasound showed persistence of the APF, with hepatofugal and pulsatile flow in the portal vein. The patient continued to have bloody emesis and melena. A transfusion was administered, and an octreotide drip was initiated. The Department of Interventional Radiology was then consulted. Hepatic angiography revealed a communication between segment VIII of the right hepatic artery and a right branch of the portal vein extending into an anomalous portal branch draining into the left portal trunk. The previously placed coils were identified in the outlet of the fistula; at the communication with the left branch of the portal vein and into a smaller peripheral radicle of the right branch of the portal vein. The APF was open with a single artery feeding a large venous aneurysm (Fig. 2A). Flow in the portal vein was hepatofugal, and there was retrograde filling of esophageal varices through the left gastric vein (Fig. 2B). Embolization of the right arterial branch that fed the APF was performed using two 5-mm × 5-cm and three 2-mm × 3-cm Gianturco coils.FIG. 2: (A) Injection of the hepatic artery showing the previously placed coils in the left branch of the portal vein (open arrow) and in a small branch of the right portal vein. The fistula is indicated with a filled arrow. (B) Venous phase showing retrograde filling of the portal venous system. Arrows indicate direction of flow. (C) Images obtained after embolization of the arterial feeder (filled arrow) showing no further communication between the hepatic artery and the portal venous system. Open arrow indicates previous embolization. (D) Arterial portogram shows hepatopetal flow in the portal vein. Arrows indicate direction of flow. Arrowhead indicates catheter in the superior mesenteric artery.An aortogram after the embolization showed no residual filling of the APF, confirming complete occlusion of the fistula, with no further filling of the portal vein (Fig. 2C). Injection of the superior mesenteric artery showed that hepatopetal flow was reestablished in the portal system (Fig. 2D). Gastroscopy performed concurrently revealed four grade II to grade III-IV esophageal varices, one exhibiting a clot; the antrum showed features consistent with portal hypertension gastropathy. There was no active bleeding. No intervention was undertaken, because it was likely that the therapeutic embolization had relieved the portal hypertension. Antral biopsy showed vascular ectasia and some increased fibrosis in the lamina propria. After arteriography, the patient had no further bleeding, and the hemoglobin remained stable. Biweekly Doppler evaluation showed no residual fistula. Flow was hepatopetal in the portal vein, but there was suspicion of an occult fistula. Persistently hemocult-positive stools prompted angiographic and endoscopic reevaluation. Celiac arteriogram revealed no evidence of APF or early venous filling that would suggest residual arterioportal communication, and there were no esophageal varices. The left hepatic artery, the splenic artery, and the inferior mesenteric artery were normal. Superior mesenteric artery injection and portal venous return showed filling of enlarged paraduodenal veins. The left branch of the portal vein was not opacified, suggesting occlusion at the site of the previous embolization by the cardiology service. Gastroscopy revealed three grade II to IV esophageal varices with no signs of bleeding. The stomach and the duodenum appeared normal. A colonoscopy to the cecum produced normal findings. Results of all biopsy specimen studies were normal. The patient was then discharged receiving nasogastric feedings, H2 blockers, and iron supplements. Two weeks later, an ultrasound examination showed no evidence of APF, decreased size of the spleen, thrombosis of the left branch of the portal vein, and the appearance of large veins in the porta hepatis. Hemoglobin, serum proteins, albumin, and liver enzymes were normal. The patient was asymptomatic and weighed 15.18 kg. Four months after the definitive embolization, his weight was 16.9 kg (75th percentile), and his height was 96.5 cm (25th percentile). He was asymptomatic, and his stools were negative for occult blood. Abdominal ultrasound again showed no evidence of residual fistula, and the size of the prominent veins in the porta hepatis had decreased. One year after the embolization, he remained well. DISCUSSION Arterioportal fistulas can be intrahepatic or extrahepatic (11-13). Although they may be congenital (1-10), they are usually acquired after blunt or penetrating trauma (14-19), percutaneous liver biopsy (19-22), transhepatic cholangiography (14,21), gastrectomy (23,24), or biliary surgery (25). They can also result from a ruptured hepatic artery aneurysm (23,26,27) or hepatocellular carcinoma (28). They may be associated with Rendu-Osler-Weber syndrome (29) or Ehlers-Danlos syndrome (14). The literature describes two common ages for presentation of congenital APFs: before the first year of life or after the fourth decade. It is often difficult to determine whether the late-onset fistulas are congenital or acquired (23). Congenital APF of the liver is rare and should be differentiated from the more common hemangioendothelioma, a vascular tumor that progresses in the first year of life and then regresses spontaneously. Hemangioendotheliomas typically have initial symptoms of high-output heart failure or isolated hepatomegaly and may be accompanied by consumption coagulopathy. Rarely, there will be shunting in the portal system. The angiographic appearance is extremely variable, ranging from relatively low-flow lesions with contrast "puddling," lesions with dense capillary blush, and lesions with direct arteriovenous or arterioportal shunting. Arteriovenous fistulas or APFs are single-hole arteriovenous communications, whereas arteriovenous malformations usually have a complex plexiform vascular nidus with multiple feeding arteries and draining veins, with or without multiple smaller arteriovenous fistulas within the nidus. Embolization of an arteriovenous fistula requires occlusion of the rent of the fistula or tract between the artery and the vein. Arteriovenous malformations are more difficult to treat, usually requiring multiple procedures, and are more prone to collateralization and recurrence after embolization. Symptoms of APF Hemodynamic Consequences Arterioportal fistula in infancy usually has an initial symptom of portal hypertension (1-3,5-7,9). Hepatofugal flow in the portal vein develops as the portal flow is arterialized. Splenomegaly, hypersplenism, esophageal varices, bleeding episodes, and ascites develop. The retrograde flow in the portal system can result in a "steal" of the flow from the superior mesenteric artery, leading to intestinal angina (1). When compared with other arteriovenous shunts, APFs are unique in that they lack propensity to result in high-output heart failure. This is thought to be related to the buffering effect of the hepatic sinusoids interposed between the lesion and the right heart (5,9,13,19,25,30,31). Occasionally, congestive heart failure may occur in infants because of associated patency of the ductus venosus. Intestinal Dysfunction Malabsorption occurs commonly (1-3,5-7,9). Intestinal dysfunction is multifactorial, in part because of venous congestion and stasis secondary to reversal of flow in the portal and superior mesenteric veins (1,2,8). High flow in the hepatic artery may compromise blood flow distal to its origin, resulting in steal of blood flow from the superior mesenteric artery if both the superior mesenteric artery and hepatic arteries originate from a common trunk. This phenomenon can result in small-bowel infarction (1). Finally, superimposed dehydration and anemia can lead to a further decrease in the mesenteric circulation, adding to the intestinal damage. Some intraoperative descriptions of the small bowel mention its congestive and cyanotic aspect (1,2,8,10). Radiologic images show edema with air-fluid levels and a malabsorptive pattern. In some cases, intestinal obstruction may be suspected (1,2,8,10). Pancreatic hypofunction, described in patients with extrahepatic portal venous obstruction, may contribute to malabsorption (32). Hepatic Dysfunction Little is known about the long-term effect on the liver of arterialized portal blood flow. Liver enzymes are usually at normal levels. The increased flow in the portal venous system may lead to the ultimate development of disease in the liver and portal vessels exposed to high-pressure flow (9,12,13,24,33). This may result in portal hypertension, despite adequate treatment. Studies, using a canine model with chronic arterialized portal circulation, have shown a variety of obliterative changes in the intrahepatic portal microvasculature, such as thickening of the walls of the portal vein, fibrosis, scarring of the portal triad, and hypertrophy of the muscularis of the portal venous radicles (34). In 1969, Donovan et al. (12) reported two patients who had hepatoportal sclerosis with portal fibrosis and thick-walled veins after chronic arterialization of the portal flow. Portal vein thrombosis after successful eradication of APFs could be secondary to the damage to the portal system induced by longstanding arterialized flow (7). Diagnosis The diagnosis of APF should be suspected in patients with unexplained portal hypertension early in life, especially when associated with malabsorption and failure to thrive, even if liver function test results appear normal. Ultrasonography with Doppler study is a noninvasive, fast, reliable diagnostic tool (3,7,8,10,30,35). The roles of computed tomographic scan and magnetic resonance imaging are still to be defined (7). Arteriography should be performed early for diagnostic purposes and possible therapy. Treatment The treatment should be aimed at occlusion of the fistula. Spontaneous closure of small acquired fistulas, has been reported (15,17-21,30) but a large congenital fistula should not be expected to close. Portosystemic shunts to relieve portal hypertension should not be part of the therapy, because they may precipitate heart failure by redirecting arterialized portal blood into the systemic venous circulation (17,18,23). Embolization is the treatment of choice in first instance (4,5,18,20,22,30,31,35-37). If necessary, it may be repeated or followed by surgical ligation of the arterial feeder. Surgical resection should be considered only when other forms of therapy fail or when the fistula is extrahepatic (2,20,30). Review There are only 11 pediatric cases of congenital APF reported in the literature (1-10) (Table 1). The present case is the 12th. Initial symptoms usually occur early in life. In the 12 cases, all except the present patient had onset of symptoms in the first year of life. Nine of 12 (75%) patients had symptoms in the first 6 months. Consequences of portal hypertension, manifested as overt gastrointestinal bleeding, were present in 11 patients (91.6%); the remaining one had only anemia and hemepositive stools. Malabsorption syndrome with diarrhea and/or failure to thrive occurred in 9 patients (75%) (1-3,5-9). Steatorrhea that resolved after ligation of the hepatic artery was documented in one case (3), and an abnormal level of D-xylose in another (6). Assessment of intestinal specimens produced normal findings in one case (3) and showed edema and increased fibrosis of the lamina propria in another (6). Intestinal symptoms can mimic intestinal obstruction, as has been reported in four cases (33.3%) (1,2,8,10). One patient (8.3%) had an initial symptom of postprandial irritability and died of small bowel ischemia secondary to steal of flow from the superior mesenteric artery (1), and one (8.3%) had heart failure (8).TABLE 1: Reported pediatric cases of arterioportal fistulaOn physical examination, hepatomegaly was noted in nine patients (75%), splenomegaly in six (50%) (1,3,5,7,9), and ascites in only two (16.6%) (3,9). A bruit or a thrill was present over the right upper quadrant in seven patients (58.3%) (2,3,5,7,8,10). Embolization alone was successful in only two patients (16.6%) (4), including the present one, but in both cases two sessions were required. Two (16.6%) had embolization followed by surgical ligation (2,9). Three (25%) had surgical ligation alone (3,8,10). One patient had surgical ligation followed by embolization (5), and one required a left hepatectomy after surgical ligation and embolization failed (7). One had resection alone (6), and one had embolization followed by left hepatectomy and subsequent ligation (9). One died without treatment. Portal vein thrombosis occurred in two patients besides ours 5 months and 2 years after definitive therapy (5,7). Our patient is unique in that the symptoms occurred late; he was asymptomatic for the first 3 years of his life. The first embolization was unsuccessful because it was directed at the outflow system of the fistula instead of the arterial feeder. Subsequent embolization of this arterial feeder resulted in complete occlusion of the fistula. The only other case in which embolization was successful required embolization of the arterial feeder and subsequent embolization of the portal outflow (4). In our case, left portal vein thrombosis resulted, which may have been related to embolization of the outflow. Embolization of the feeder artery can be curative. However it is important to continue to observe patients, because the fistula can recur through arterial collateralization. There is a risk of portal vein thrombosis with recurrence of symptoms of portal hypertension after successful eradication of the APF (5,7), and therefore, the option of posttreatment anticoagulotherapy should perhaps be raised.