DOI: 10.1148/radiol.2473070529
(Radiology 2008;247:880-886.)
© RSNA, 2008
Vascular and Interventional Radiology |
Hepatic Arterial Injuries after Percutaneous Biliary Interventions in the Era of Laparoscopic Surgery and Liver Transplantation: Experience with 930 Patients1
Nicholas Fidelman, MD,
Allan I. Bloom, MD,
Robert K. Kerlan, Jr, MD,
Jeanne M. LaBerge, MD,
Mark W. Wilson, MD,
Ernest J. Ring, MD, and
Roy L. Gordon, MD
1 From the Department of Radiology, University of California, San Francisco, 505 Parnassus Ave, Room M-361, San Francisco, CA 94143. Received March 21, 2007; revision requested May 23; revision received August 17; accepted September 19; final version accepted October 29.
Address correspondence to A.I.B., Department of Radiology, Hadassah University Medical Center, Kiryat Hadassah, Jerusalem il-91-120, Israel (e-mail: Allan{at}hadassah.org.il).
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ABSTRACT
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Purpose: To retrospectively determine if patients with a history of intraoperative bile duct injury or liver transplantation have an increased risk for arterial injury (AI) during percutaneous transhepatic cholangiography (PTC) and percutaneous transhepatic biliary drainage (PTBD) compared with the risk of AI established in the 1970s and 1980s.
Materials and Methods: This study was approved by the committee on human research and was deemed compliant with the Health Insurance Portability and Accountability Act. The informed consent requirement was waived. Records of 1394 procedures (307 PTCs, 1087 PTBDs) performed in 930 patients (445 male, 485 female; age range, 4 months to 99 years) over the past 13 years were retrospectively reviewed. The rate of AI was determined, and demographic, pathologic, technical, and laboratory variables were tested for association with increased risk of AI by using generalized estimating equation analysis.
Results: AIs were encountered after 30 (2.2%) biliary procedures. No significant difference in the rate of AI was seen among the groups of patients with malignant biliary obstruction (1.8%), history of bile duct injury (2.2%), or complications of liver transplantation (2.6%). Patients who underwent PTBD had a higher risk of AI than did patients who underwent PTC (2.6% vs 0.7%); however, this difference was not significant (P = .06). Ongoing hemobilia was seen in 26 (87%) of the patients, which made it the most common sign of AI, and it had a 94% positive predictive value for AI. A postprocedure decrease in the hematocrit level of more than 13% was seen only in the setting of AI, and it occurred in only three (10%) of patients with AIs.
Conclusion: PTC and PTBD performed for management of bile duct injury and complications of liver transplantation are not associated with an increased risk of hepatic AIs compared with the risk of AI reported in the 1970s and 1980s.
© RSNA, 2008
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INTRODUCTION
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Percutaneous transhepatic cholangiography (PTC) remains an important tool in bile duct imaging, while percutaneous transhepatic biliary drainage (PTBD) has an established role in the diversion of bile flow in the setting of biliary obstruction or leakage (1). In the 1970s and 1980s, 65%–92% of patients undergoing PTC or PTBD had a malignant cause of biliary obstruction (2–7). Between 1% and 12% of patients had intraoperative bile duct injuries (2–5,7,8), whereas patients with complications of liver transplantation were encountered infrequently. Changes in the patient population undergoing PTC and PTBD occurred after the advent of endoscopic retrograde choledochopancreatography, laparoscopic cholecystectomy, and liver transplantation, which have become commonplace. Many patients with malignant diseases now undergo endoscopic retrograde choledochopancreatography, while many patients with laparoscopic bile duct injuries and complications of liver transplantation are referred for percutaneous procedures (9).
To our knowledge, the risk of hemorrhage resulting from PTC and PTBD has not been reassessed since the older retrospective series on this topic was published (1). In the 1970s and 1980s, rates of substantial hemorrhage in the form of hemobilia, subcapsular hematoma, and hemoperitoneum that required surgery or angiography with embolization ranged from 1.3% to 8.0% (3–8,10,11). Quality improvement guidelines for PTC and PTBD published in 2003 (1) indicated a 2.5% average rate of hemorrhage and suggested an acceptable threshold rate of 5.0%. These guidelines, despite their relatively recent publication, were based on data obtained in the 1970s and 1980s. To our knowledge, no recent large series examining the rate of arterial injury (AI) in patients referred for intraoperative bile duct injuries and complications of liver transplantation has been published.
We hypothesized that patients with intraoperative bile duct injuries and complications of liver transplantation often have bile leakage, nondilated ducts, or both and are therefore less likely than patients with malignant obstruction to have intrahepatic biliary ductal dilatation. The smaller size of these target ducts, together with a tendency to have multiple needle passes and more central bile duct puncture, may predispose patients to AI. Thus, the purpose of our study was to retrospectively determine if patients with a history of intraoperative bile duct injury or liver transplantation have an increased risk for AI during PTC and PTBD compared with the risk of AI established in the 1970s and 1980s.
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MATERIALS AND METHODS
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Patients and Study Outcomes
Our retrospective study was approved by the committee on human research at our institution and was deemed compliant with the Health Insurance Portability and Accountability Act; the informed consent requirement was waived. A search of our department of radiology database, which contained comprehensive records of diagnostic examinations dating back to January 1, 1993, was performed to identify all PTC and PTBD procedures performed at our institution and an affiliate hospital between January 1, 1993, and April 15, 2006. Only biliary interventions that required needle puncture of liver parenchyma were included. Biliary tube changes and nonbiliary percutaneous transhepatic procedures were excluded. In all, 1394 procedures (307 PTCs, 1087 PTBDs) were performed in 930 patients (445 male, 485 female; age range, 4 months to 99 years; mean age, 54.5 years ± 18.0 [standard deviation]).
The main study outcome was hepatic AI depicted at digital subtraction angiography. Clinical signs of AI included systemic hypotension (systolic blood pressure less than 90 mm Hg), substantial hemobilia, enlarging subcapsular liver hematoma, expanding hemothorax, and decrease in hematocrit level of at least 5% (12). For the purpose of this review, substantial hemobilia was defined as bleeding from or around the biliary catheter lasting at least 12 hours, brisk hemorrhage along the catheter track encountered at the time of tube exchange, or melena or hematemesis observed within 1 week of the biliary procedure.
Risk Factors for Hemorrhage
Potential effects on the rate of AI from a number of demographic, technical, laboratory, and pathologic factors were investigated. Two authors (N.F., A.I.B.) collected data. Data were obtained from the electronic medical records (discharge summaries, clinic notes, and imaging and procedure reports). Patients' age and sex were among the demographic factors. Technical factors included type of procedure performed (PTC or PTBD), side of puncture (right or left), use of ultrasonography (US) for needle guidance, needle gauge, drainage catheter diameter, number of drainage catheters placed during PTBD on a given day, and identity of the radiologist who performed the procedure. Data on the side of puncture, US guidance, number of inserted catheters, and operator identity were available for all procedures. Information regarding needle size was available for 1042 (74.7%) procedures. Tube size could be obtained for 914 (84.1%) PTBDs. Data on the number of needle passes required to gain access to the bile ducts were not available in this retrospective review. Information regarding the cause of biliary obstruction, presence or absence of intrahepatic biliary ductal dilatation, cirrhosis, ascites, or intrahepatic tumor at the time of PTC or PTBD was available for all patients.
Laboratory data obtained before and after PTC or PTBD were available for 1287 (92.3%) procedures. Preprocedure platelet count, hematocrit level, prothrombin time, international normalization ratio, and partial thromboplastin time were recorded. Hematocrit levels obtained within 3 months of the procedure were reviewed to determine if a hematocrit decrease of more than 5%, which could have been attributed to the procedure, had occurred (12). On the basis of our department guidelines, patients were required to have a maximum international normalization ratio of 1.5, a minimum hematocrit level of 25%, and a minimum platelet count of 50 000 per milliliter prior to undergoing biliary intervention. Appropriate transfusions were administered if preprocedure laboratory values did not meet these standards.
Two authors (N.F., A.I.B.) analyzed images obtained during PTBD that led to AI to determine if the site of tube insertion affected the risk of AI. Images were available for 23 (77%) of the 30 biliary procedures that resulted in AIs. Images from these 23 studies were compared with images from 30 procedures that did not result in hemorrhage. The control studies were matched for side of puncture, cause of obstruction, presence of duct dilatation, needle gauge, and tube size.
All patients who underwent digital subtraction angiography after PTC or PTBD were identified by searching the radiology department database. Two authors (N.F., A.I.B.) reviewed the angiography reports to determine which examinations were performed to assess hemorrhage resulting from antecedent biliary procedures. Thirty-two relevant hepatic artery angiography examinations were performed in patients suspected of having an AI. Angiographic images were available for 23 (72%) of these examinations. Indications for angiography, type and location of angiographic abnormalities, requirements for transcatheter embolization, and patient outcomes (ie, resolution of hemorrhage, surgery, or death) were recorded. For analysis purposes, ducts and arteries originating from the common hepatic duct and common hepatic artery were classified as zero-order structures. Each subsequent branching point increased the order of the duct or artery by one. In data analysis, zero- and first-order structures were considered central structures, whereas second-order or higher structures were classified as peripheral structures.
Statistical Analyses
Statistical analyses were performed with respect to the main study outcome of AI. A null hypothesis was assumed for all statistical comparisons. Because of the large number of patients who underwent multiple procedures, a univariate generalized estimating equation model (SAS, version 9.1; SAS Institute, Cary, NC) was used to evaluate the effects of a number of potential risk factors for AI. Variables analyzed with the univariate generalized estimating equation model included type of procedure performed (PTC or PTBD); patients' sex and age; cause of biliary obstruction; presence of ductal dilatation, cirrhosis, ascites, or suspected puncture through tumor in liver parenchyma; side of puncture; use of US guidance; site of tube insertion; tube size; needle gauge; operator experience; and patients' prothrombin time, international normalization ratio, partial thromboplastin time, platelet count, and hematocrit level. Generalized estimating equation analysis was also used to compare the number of patients with and without AI with respect to the presence of coagulopathy, thrombocytopenia, severe anemia, and pre- or postprocedure transfusion requirements.
The association between AI and the number of biliary drainage catheters inserted in 1 day was evaluated with the 
2 test (Excel; Microsoft, Redmond, Wash). The 2 test was also used to test for an association between AI and biliary drain insertion into a central duct, as well as an association between substantial decrease in the hematorcit level and the presence of AI. The degree of decrease in the hematocrit level and the time between a biliary procedure and a nadir in the hematocrit level were analyzed with the two-tailed Student t test (Excel). The null hypothesis was rejected if P values were less than .05.
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RESULTS
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Procedures
Referrals for malignant diseases accounted for 499 (35.8%) of the 1394 procedures, while 372 (26.7%) and 271 (19.4%) procedures were performed for evaluation and management of complications related to liver transplantation and intraoperative bile duct injury, respectively (Table 1). The remaining 252 (18.1%) biliary procedures were performed for other benign indications, such as choledocholithiasis, pyogenic cholangitis, primary sclerosing cholangitis, congenital or other benign biliary strictures, and evaluation of chronic abdominal pain. Successful opacification of the bile ducts was achieved in 288 (93.8%) of 307 PTCs. Biliary drainage was established as a result of 1085 (99.8%) of the 1087 PTBDs. In two procedures, the ducts were opacified with contrast material, but catheterization could not be performed.
Number of AIs
Angiography was performed to evaluate ongoing hemorrhage after 32 (2.3%) of 1394 biliary interventions. Hepatic AIs were seen on 30 (94%) angiograms obtained in 32 patients. The overall rate of AI in the study population was 2.2%. No significant differences in the rates of AI were seen after (a) 271 procedures performed to evaluate intraoperative bile duct injuries, (b) 372 procedures performed in patients with complications stemming from liver transplantation, or (c) 499 biliary interventions performed to manage malignant biliary obstruction; rates of AI were 2.2%, 2.6%, and 1.8%, respectively (P = .65). Twenty-six (87%) of the 30 patients with AI presented with substantial hemobilia, whereas only two (0.2%) of the 900 patients without AI had substantial hemobilia after biliary procedures. Thus, substantial hemobilia had a 94% positive predictive value for hepatic AI at angiography. Nine (30%) of the 30 patients with AI had decreased bile output from the tube. These patients developed brisk bleeding from the catheter track at the time of catheter exchange. Other clinical signs of AI are summarized in Table 2.
AIs were detected within 2 days of biliary intervention in six (20%) of 30 patients with AI. In the remaining 24 (80%) patients, AI was diagnosed between 3 and 71 days after PTC or PTBD (Table 2). There was a significant (P = .001) trend toward diagnosing AI 3 or more days after biliary intervention. Substantial hemobilia was the most common sign of AI, irrespective of the interval between biliary intervention and onset of bleeding.
The most common angiographic findings in the 30 patients with AIs were active contrast material extravasation in 13 (43%), hepatic artery branch pseudoanurysms in 13 (43%) (Fig 1), and arteriocholedochal fistulas in 10 (33%) (Fig 2). Fistulas extending from the hepatic artery to the portal vein were seen on three angiograms (10%) (Fig 3). In all patients with AI, damage to the peripheral hepatic artery branches occurred (Table 2).
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Figure 2: Anteroposterior digital subtraction angiogram obtained after partial retraction of the biliary drain shows a fistula extending from the left hepatic artery branch (arrows) to the bile duct (arrowheads).
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Figure 3: Anteroposterior digital subtraction angiogram obtained in a patient with a concomitant hepatic artery pseudoaneurysm (long arrow) shows a fistula extending from the right hepatic artery (short arrows) to the right portal vein (arrowheads).
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Transcatheter arterial embolization with coils was used to successfully control bleeding in 29 (97%) of 30 patients with AI. In one patient, an arterial branch supplying a vessel with a small pseudoaneurysm could not be identified, and embolization was not attempted. Bleeding resolved spontaneously in this patient. There were no deaths that were directly attributable to hemorrhage. Surgery was required in one patient who sustained injuries to the right 10th intercostal artery and to a peripheral branch of the right hepatic artery. In this patient, hepatic AI was treated with transcatheter embolization, while trauma to the intercostal artery was managed surgically. In addition to angiography and embolization, existing biliary catheters were exchanged for larger-bore drains in five (17%) of the 30 patients with AI (Table 2).
Factors Evaluated
A number of demographic, pathologic, technical, and hematologic factors were tested for potential association with an increased rate of AI (Table 3). The rate of AI after 307 PTCs was 0.7%, which was not significantly lower (P = .06) than the rate of AI after 1087 PTBDs (2.6%). Lack of biliary ductal dilatation, cirrhosis, ascites, or extensive intrahepatic parenchymal metastases was not associated with an increased rate of AI. A significant increase in the rate of AI was associated with use of large-bore (18-gauge sheathed) needles (P = .001) and with placement of three drainage catheters on the same day (P = .001). Biliary procedures performed via the left lobe, puncture of central ducts, interventions performed without US guidance, and insertion of larger-bore (10- or 12-F) drainage catheters were not associated with a significant increase in the rate of AI (Table 3).
A decrease in the hematocrit level of more than 5% was observed after 50 (3.6%) of the 1394 biliary procedures and was more common after procedures that resulted in AI (six [20%] of 30 procedures) than after procedures that did not result in AI (44 [3.2%] of 1364 procedures, P < .001). The percentage decrease in the hematocrit level ranged from 6.4% to 27.6% in patients with AI and from 5.0% to 12.2% in patients without AI (Table 3). A decrease of more than 13% in the hematocrit level was observed only in three patients with AIs.
Five attending physician operators (R.K.K., J.M.L., M.W.W., E.J.R., R.L.G.) performed 1286 (92.3%) of the 1394 procedures. Individual operator-related rates of AI ranged from one in 131 biliary procedures (0.8%) to six in 174 biliary procedures (3.4%) and did not vary significantly among the operators (Table 3). Four of the five physicians had 12–16 years of experience with biliary interventions when the study period commenced. The fifth physician completed training after the study period had begun; therefore, this operator had less experience with biliary interventions. However, we did not observe an increase in the number of hemorrhagic complications caused by the less experienced attending radiologist.
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DISCUSSION
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In the 1970s and 1980s, 65%–92% of patients referred for PTC or PTBD had a diagnosis of malignant biliary obstruction, while iatrogenic biliary complications accounted for only 1%–12% of the referrals (2–5,7,8). Over the past 13 years, only 499 (35.8%) procedures were performed for malignant diseases, whereas complications of liver transplantation and bile duct injuries accounted for 372 (26.7%) and 271 (19.4%) procedures, respectively. Despite changes in the patient population, the overall rate of hepatic AI in this study was 2.2%, which was largely unchanged from the AI rate reported previously (1). There was no significant difference in the rate of AI among patients with malignant biliary obstruction, those with a history of bile duct injury, and those with complications of liver transplantation.
A 3.7-fold higher rate of AI was observed after PTBD than after PTC. This may have been due to a higher risk of injury to the hepatic artery associated with multiple catheter and wire manipulations prior to drainage tube insertion. The delayed presentation of AI may have been explained by an initial tamponade effect of a biliary catheter on the injured hepatic artery branch.
Substantial hemobilia was the most common clinical sign of AI (87%). Evidence of substantial blood loss revealed by postprocedure laboratory studies was not a consistent predictor of AI. Thus, only six of 50 patients who had a substantial decrease in their hematocrit level had an AI. However, the patients with an AI had a significantly more profound degree of blood loss compared with patients with self-limited bleeding (average hematocrit decrease, 13.5% vs 7.3%; P < .001). These findings suggest that self-limited blood loss after a biliary intervention may have been caused by an injured venous structure or a relatively minor AI.
Associations between a number of technical, pathologic, and hematologic factors and risk of bleeding after PTC or PTBD have been proposed in the literature. However, to our knowledge, no significant association was previously demonstrated between the rates of AI and the side of puncture (9), clotting abnormalities, or elevated liver function test results (11). L'Hermine et al (7) found a significantly higher rate of hemorrhage in patients with a benign cause of biliary obstruction. We could not confirm this association. Goodwin et al observed a decreased rate of hemobilia when potential biliary drainage tracks were abandoned once a major hepatic vessel was seen on needle (13) or sheath (14) cholangiograms. This technique is not used routinely at our institution.
We anticipated that the presence of intrahepatic biliary dilatation might result in a lower incidence of hemorrhage because of the larger target duct, which would require fewer needle passes to access it. Similarly, more dilated ducts should facilitate a more peripheral duct puncture, which might reduce the likelihood of injury to a larger branch artery. For the same reasons, we postulated that patients with benign disease and nondilated ducts would be at higher risk for developing substantial bleeding compared with patients with malignant disease and dilated ducts. In practice, however, we found that small duct size and benign indications for biliary procedures were not associated with increased rates of AI. In this series, there appeared to be an increased risk of AI after the use of 18-gauge sheathed needles and after insertion of three tubes at the time of biliary drainage. However, no significant increase in the rate of AI was seen for larger-caliber (10- or 12-F) drains.
Our study had limitations. Because of the retrospective study design, data on the various technical, pathologic, and hematologic risk factors were limited to the subset of records that contained such information. It is possible that some of the patients who underwent biliary interventions at our institution received treatment for AIs elsewhere. There may be a causal relationship between the number of needle passes required to opacify the ducts and the incidence of AI. We could not retrospectively determine the number of passes required to access the ducts. Variations in the technique over the past 13 years also could have influenced the results. For instance, while 18-gauge sheathed needles frequently were used at the beginning of the study period, they were phased out over the past 10 years, and 21- or 22-gauge needles are now used almost exclusively for bile duct access. However, no significant decrease in the risk of AI was noted after use of 18-gauge sheathed needles was discontinued.
In conclusion, despite changes in the patient population and alterations in the technique used for PTC and PTBD, the risk of hepatic AI over the past 13 years has remained similar to that established in the 1970s and 1980s. Hepatic AIs frequently manifest weeks or even months after biliary drain placement. AIs occurred more often after PTBD than after PTC, especially if three catheters were inserted in 1 day and when 18-gauge sheathed needles were used for bile duct access. Clinical signs of substantial hemobilia had a high correlation with demonstrable AI at angiography.
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ADVANCES IN KNOWLEDGE
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- The risk (2.3%) of procedure-related hepatic arterial injuries (AIs) has not changed since the 1970s and 1980s.
- The risk of AI in patients with no intrahepatic biliary ductal dilatation (2.0%) was similar to that in patients with biliary obstruction and dilated intrahepatic bile ducts (2.2%).
- Percutaneous transhepatic biliary drainage (PTBD) carried a 3.7-fold higher risk of AI than did percutaneous transhepatic cholangiography (PTC).
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IMPLICATIONS FOR PATIENT CARE
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- Use of 18-gauge sheathed needles and insertion of three biliary catheters on the same day were associated with an increased risk of hepatic AI.
- Substantial hemobilia (defined as prolonged bleeding from or around the catheter, brisk bleeding along the catheter track during tube exchanges, melena, and hematemesis) had a 94% positive predictive value for hepatic AI.
- A decrease in the hematocrit level of more than 13% after PTC or PTBD was observed only in the setting of AI but was found in just 10% of patients with AI.
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ACKNOWLEDGMENTS
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We are grateful to Diane O. Inglis, PhD, for critical reading of the manuscript.
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FOOTNOTES
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Abbreviations: AI = arterial injury • PTBD = percutaneous transhepatic biliary drainage • PTC = percutaneous transhepatic cholangiography
Author contributions: Guarantors of integrity of entire study, N.F., A.I.B.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, N.F., A.I.B.; clinical studies, all authors; statistical analysis, N.F., A.I.B., J.M.L.; and manuscript editing, all authors
Authors stated no financial relationship to disclose.
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References
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ABSTRACT
INTRODUCTION
