Delayed Fatal Hemorrhage From Pseudoaneurysmof the Hepatic Artery After Percutaneous Liver BiopsyAijaz Ahmed, M.D., Shaun L. Samuels, M.D., Emmet B. Keeffe, M.D., Ramsey C. Cheung, M.D.Division of Gastroenterology and Department of Radiology, VA Palo Alto Health Care System, Palo Alto,California; and Division of Gastroenterology, Stanford University School of Medicine, Stanford, California

ABSTRACTHemorrhage is the most common serious complication ofpercutaneous liver biopsy. Liver biopsy is usually done in anoutpatient setting because most significant hemorrhage isevident within a few hours after biopsy. Delayed hemor-rhage occurs much less frequently but carries a much highermortality. We present a 41-yr-old man with chronic hepatitisC who underwent a percutaneous liver biopsy uneventfullybut was found to have a pseudoaneurysm of the hepaticartery 5 days later. Shortly after admission, the patientexperienced bleeding into the liver from the pseudoaneu-rysm, which was controlled initially by angiographic em-bolization. However, recurrent bleeding could not be con-trolled by repeat angiography and surgical intervention, andthe patient expired. The diagnosis and management of pseu-doaneurysm of the hepatic artery complicating liver biopsyis reviewed. (Am J Gastroenterol 2001;96:233–237. © 2001by Am. Coll. of Gastroenterology)

INTRODUCTION

Percutaneous liver biopsy (PLBx) is a relatively safeprocedure for the evaluation of chronic liver diseases.The most common complication of PLBx is bleeding. Therisk of fatal hemorrhage is 0.4% in patients with malig-nancy and 0.04% in nonmalignant liver diseases (1). Themajority of bleeding complications after PLBx occurearly and are recognized before discharge from the hos-pital or ambulatory unit. The less common complicationof delayed bleeding,i.e., days to weeks after PLBx, hasa higher mortality associated with late recognition (2). Anuncommon cause of delayed hemorrhage is pseudoaneu-rysm of the hepatic artery. Pseudoaneurysms of the he-patic artery initially should be managed with angio-graphic embolization, reserving surgical intervention forfailure of embolization (3). We present a case of fataldelayed hemorrhage from pseudoaneurysm of the hepaticartery after PLBx, despite early diagnosis followed byangiographic and surgical intervention.

CASE REPORT

A 41-yr-old man was evaluated for progressive fatigue andelevated aminotransferases. He had a history of intravenousdrug use and was positive for antibody to hepatitis C virus(HCV) by a second-generation enzyme immunoassay andalso for HCV RNA by polymerase chain reaction. Otheretiologies of chronic liver disease were excluded by appro-priate blood tests. Physical examination was unremarkable.The complete blood count, including platelet count, andcoagulation studies were normal. Abdominal ultrasoundwas normal and showed no evidence of cirrhosis or a focalhepatic lesion. The patient had a PLBx to complete baselineevaluation before interferon therapy. A PLBx was per-formed with a 16-gauge Klatskin needle using the Menghinitechnique with one pass. The procedure was uneventful, andthe patient remained hemodynamically stable and was dis-charged home after 6 h of observation. The liver biopsyspecimen showed chronic hepatitis with grade 2 of 4 necro-inflammatory activity and stage 2 of 4 fibrosis.

Four and one-half days after PLBx, the patient presentedto the emergency department complaining of sudden onsetof right upper quadrant pain radiating to the right shoulder.The pain had started 1 h before presentation. The patientdenied nausea, vomiting, dizziness, shortness of breath, orabdominal trauma. He was afebrile with blood pressure (BP)150/80 mm Hg, heart rate (HR) 58 beats/min, and respira-tory rate (RR) 12 breaths/min. The abdomen was soft withnormal bowel sounds and mild right upper quadrant tender-ness without rebound tenderness or rigidity. Laboratory datarevealed a white blood cell count of 5800/ml, Hct 49%,platelets 208,000/ml, prothrombin time international nor-malized ratio (INR) 1.1, aspartate aminotransferase (AST)101 IU/L, alanine aminotransferase (ALT) 140 IU/L, andtotal bilirubin 0.7 mg/dl. BUN and creatinine were normal.The complete blood count and liver tests were similar topatient’s baseline values. An emergency abdominal ultra-sound with Doppler revealed a 4.83 3.1 3 3.8 cm intra-hepatic pseudoaneurysm superior to the gallbladder at theinterlobar region with no evidence of subcapsular or peri-toneal bleed. The patient suddenly became hemodynami-cally unstable with a HR 140 beats/min and BP 80/40 mmHg 15 h after admission, which was over 6 days after thePLBx. The extremities were cold and clammy, accompanied

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by increasing abdominal distention. The repeat Hct was37%. The patient was resuscitated and underwent immediateangiography, which showed a pseudoaneurysm in the righthepatic artery branch (Fig. 1A) with active extravasationfrom the right superior lateral aspect of the liver into thesubcapsular space. A parenchymal tract to the liver capsulewith extravasation into the perihepatic space was identified.A mass effect was noted with medial deviation of the lateralaspect of the liver.

The patient was treated with embolization using multiplestraight and helical coils along the length of the right hepatic

artery branch (Fig. 1B). There was no active bleeding at theend of procedure. Over the next 15 h, the patient wasresuscitated with blood products, administered dopaminefor decreasing urine output, and intubated for increasingoxygen requirement. Because of constant transfusion re-quirements, angiogram was repeated 30 h after admissionand revealed continued extravasation of blood from the rightlateral subcapsular location. The angiogram demonstratednew areas of active arterial extravasation (Fig. 1C) withpossible complex laceration of right hepatic lobe, not ame-nable to embolotherapy. The laboratory values obtained

Figure 1. (A) Subselective arteriogram of a branch of the right hepatic artery. Microcatheter (small arrows) within right hepatic artery withbeaded tip (large arrow) just proximal to pseudoaneurysm (arrowheads). The pseudoaneurysm measures approximately 1.53 2 cm. (B)Hepatic arteriogram obtained after embolization of the branch leading to and from the pseudoaneurysm. Platinum coils (solid arrows) areseen filling the feeding branch. A relative paucity of vessels is seen in the medial segment of the left lobe (empty arrows) representinga parenchymal hematoma.(C) Repeat arteriogram after initial embolization shows a large subcapsular hematoma has formed. Multiplesmall bleeding vessels (arrowheads), not seen on prior arteriogram, have developed and are seen extending into this hematoma. Anoccluded posterior segment branch is now seen (curved arrow), probably secondary to spasm. The left lobe parenchymal hematoma is againseen (straight lines). Coils are shown by straight arrows.

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approximately 36 h after admission showed AST 5050 IU/L,ALT 4080 IU/L, alkaline phosphatase 280 IU/L, total bili-rubin 1.4 mg/dL, INR 2.2 despite constant infusion of freshfrozen plasma, albumin 1.6 g/dl, creatinine 2.1 mg/dl, andBUN 18 mg/dl. The patient was taken to the operating room,and laparotomy revealed a stellate right hepatic lobe lacer-ation with hemorrhage. The laceration was oversewn andpacked. After surgery, patient continued to deteriorate clin-ically with a decreasing Hct. Repeat ultrasound of the ab-domen revealed the interval development of multiple cysticlesions in the right hepatic lobe compatible with intrahepatichematomas, and a large free intraperitoneal (i.p.) fluid col-lection. Over the next 3 days, the patient was taken back tothe operating room 2 more times. No active bleeding fromthe liver was seen either time, but diffuse oozing of bloodwas noted from the liver, muscle, and fascia. No furthersurgical intervention was performed because of the diffusenature of the bleeding. The patient died 5 days after admis-sion from multiorgan failure. Autopsy showed numerousfoci of necrosis throughout both lobes of the liver, with theright lobe almost entirely necrotic. There was a large he-matoma measuring approximately 103 8 3 5 cm extendingfrom the left lobe of the liver in the hilar region to theproximal portion of the right lobe (Fig. 2).

DISCUSSION

The most common indication for percutaneous liver biopsyat our institution is for evaluation of chronic hepatitis C.According to the recent National Institutes of Health con-sensus conference on the management of chronic hepatitisC, liver biopsy is recommended before therapy to assess theseverity and activity of the liver disease (4). Treatment withinterferon is recommended if the liver biopsy shows evi-dence of septal fibrosis and/or moderate-to-severe necroin-flammatory changes.

Percutaneous liver biopsy is a relatively safe procedureand is usually performed in an outpatient setting (5, 6). Only3.2% of patients required admission after outpatient liverbiopsy at Mayo Clinic, and the average length of stay was1.5 days (7). A review combining several series showed anoverall complication rate of 0.28% and fatality rate of 0.03%among 189,085 liver biopsies (8). In the two largest reportedseries, there were 3 deaths in 68,276 (0.004%) and 19 deathsin 36,786 (0.052%) biopsies (9). Early bleeding withinhours can result from intrahepatic hematoma or laceration ofthe liver capsule (1), and hemorrhage either within or ex-ternally from the liver is the most common reason for a fatalcomplication associated with PLBx (10). In the largest U.S.series, there were 32 (0.35%) major hemorrhages, resultingin 10 deaths among 9212 liver biopsies performed at theMayo Clinic over 20 yr (1). Significant hemorrhage wasevident within 3 h after PLBx in all patients. Factors asso-ciated with an increased risk of hemorrhage included in-creasing age, number of biopsy passes (1) and presence ofmalignancy in the liver (1, 11). Increased risk was notrelated to location of puncture, operator experience, or in-patient/outpatient status (1). The risk of hemorrhage (1) orcomplication (12) also was not related to the biopsy needletype or diameter of the needle (13). Older patients withmalignant disease undergoing multiple liver biopsies werethe group with the highest risk for fatal (0.4%) and nonfatal(0.6%) bleeding complications (1). Bleeding complicationafter PLBx was lower (0.04% fatal and 0.16% nonfatal)among patients with nonmalignant liver disease (1). Mildcoagulopathy (prothrombin time up to 1.5 times control orpartial thromboplastin time up to 2.0 times control or plate-let count of 50–993 109/L) were not associated withincreased risk of hemorrhage (11), but bleeding was morecommon if the INR was.1.5 (7.1%vs3.3% when INR51.3–1.5) (12). Reichertet al. in 1983 found only 15 cases ofdelayed hemorrhage after PLBx in the world literature, withhemorrhage occurring 36 h to 18 days after liver biopsy. Sixof these 15 patients died.

This case report demonstrates an unusual complication ofhepatic artery pseudoaneurysm from PLBx. Pseudoaneu-rysms more commonly occur in patients who are post livertransplant (14) or post cholecystectomy (15, 16). There wereonly 11 pseudoaneurysms among 1211 patients undergoingmultiple liver biopsies after liver transplantation, but only 2cases (0.17%) were attributed to PLBx (14). However, astudy in rabbits demonstrated that hematomas, hemorrhage,pseudoaneurysms, and arteriovenous (AV) fistulas occur inup to 50% of the animal undergoing PLBx, provided an-giogram is performed immediately (17). After PLBx inhumans, angiographic defects (AV fistulas, pseudoaneu-rysms, hematomas, and occluded arteries) were found in61% of angiograms performed within 1 wk but in 11% ofangiograms done after more than 1 wk, suggesting rapidhealing (18). Most patients experiencing these events areasymptomatic. The pseudoaneurysms and AV fistulas eitherheal spontaneously (3) or remain asymptomatic for long

Figure 2. At autopsy, there was a large hematoma measuringapproximately 103 8 3 5 cm extending from the left lobe of theliver (indicated by the knife) in the hilar region to the proximalportion of the right lobe. There were also numerous foci of necrosisthroughout both lobes.

235AJG – January, 2001 Fatal Hemorrhage After Liver Biopsy

periods, followed by complications of portal hypertension(19).

A pseudoaneurysm does not have an endothelial liningbut represents a cavitated hematoma associated with focalarterial defect. The clinical features of pseudoaneurysmsand AV fistulas may range from no symptoms to hemobiliato massive delayed fatal hemorrhage, as reported in thiscase. Patients with hemobilia usually present with colickyright upper quadrant pain, intermittent jaundice, and GIbleeding (Quincke’s triad, which is seen in only one-third ofthe cases (15). Ultrasound with Doppler can be used todiagnose pseudoaneurysm and AV fistula and to evaluateportal blood flow. Pseudoaneurysms can be missed by non-contrast computerized tomography (CT) studies (14), anddynamic contrast-enhanced CT scan is recommended (20).Selective visceral arteriogram is the diagnostic procedure ofchoice in patients with negative CT scan and with highclinical suspicion. A celiac or selective hepatic angiogramwill demonstrate the actual location and size of the pseudo-aneurysm (16, 21).

Goldblatt et al. (22) reported 3 patients with hepaticartery aneurysm who underwent hepatic artery ligation. Twoof the three patients died after the procedure, and the thirdhad major postoperative complications from partial hepa-tectomy. In contrast to surgery, embolization is performedunder local anesthesia with precise localization of the bleed-ing site. In 7 reports comprising 34 patients, embolization ofa hepatic artery pseudoaneurysm had a success rate of 97%(15). Potential complications of therapeutic embolizationinclude infection, retrograde propagation of the thrombus,and accidental embolization of other arteries (23). The oc-clusion of the more proximal hepatic artery caused by dis-section or thrombosis may necessitate a direct percutaneousapproach (15). Hepatic failure is a life-threatening compli-cation of embolization in cirrhotics (23). Both transarterialand direct percutaneous access to pseudoaneurysms havealso been successfully employed (15). The embolotherapyinvolves exclusion of the pseudoaneurysm by embolizationof the distal and proximal feeding arteries to the neck of theaneurysm. However, direct embolization of the pseudoan-eurysm, allowing patency of the hepatic artery, has alsobeen reported (15). Pseudoaneurysm with large cavity maybe best managed by adequate debridement with ligation ofthe pseudoaneurysm (24). It may be appropriate to performformal hepatic lobectomy, eliminating both pseudoaneu-rysm and large cavity. The potential for blood loss is lesswith lobectomy along anatomic lines of dissection than withattempted debridement of the large cavity (3). The use ofdeep mattress sutures for initial control of bleeding is notrecommended; omental packing in tamponading venousbleeding is preferred (25). In this case, bleeding from pseu-doaneurysm of the hepatic artery was controlled initiallywith embolization, but patient continued to deteriorate fromrebleeding. In retrospect, bleeding might have been bettercontrolled with immediate surgical exploration.

In conclusion, pseudoaneurysm of hepatic artery is anunusual complication after percutaneous liver biopsy. Thiscomplication can result in delayed fatal hemorrhage despiteearly diagnosis. Pseudoaneurysms should initially be man-aged with angiographic embolization (3), but surgical inter-vention may be needed if embolization fails. Hepatic lobec-tomy or debridement accompanied by ligation of thepseudoaneurysm are the two surgical approaches that havebeen successfully employed (3, 24). Close, coordinated,periodic follow-up by the surgery and radiology team canlead to early diagnosis of pseudoaneurysms refractory toembolotherapy and aggressive surgical therapy. Dependingon local expertise, immediate laparotomy might also beappropriate because there might only be a small “window ofopportunity” to save the patient.

Reprint requests and correspondence:Ramsey C. Cheung,M.D., Division of Gastroenterology, VA Palo Alto HCS, 154C,3801 Miranda Avenue, Palo Alto, CA 94304.

Received Dec. 31, 1998; accepted Apr. 8, 1999.

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