Sheldon B. Kaplan, MD • Albert B. Zajko, MD • Baburao Koneru, MD 2
Hepatic Bilomas Due to Hepatic Artery Thrombosis in Liver Transplant Recipients: Percutaneous Drainage and Clinical Outcome' During the past 4 years, the authors performed catheter drainage in 15 patients (five adults and 10 children) with 16 hepatic allografts who had intrahepatic bilomas after occlusion of the hepatic artery. Ten of the 16 (62%) allografts (in four adults and six children) were replaced within 4 months of drainage: Nine were replaced because of biliary sepsis or abscess, and one was replaced because of the absence of biliary-enteric communication. Most of these patients had cholangiographic evidence of extensive bile duct necrosis. In two patients, retransplantation was avoided for longer than 2 years. One of these needed a new liver because of multiple central biliary strictures. Four patients have now lived for 30-44 months since initiation of drainage without needing new livers. Despite drainage, the outcome of most of these allografts has been poor. However, in some liver transplant recipients who have had hepatic artery thrombosis, biloma drainage can prolong allograft survival and prevent retransplantation. Index terms: Bile ducts, interventional procedure, 76.1229 • Bile ducts, leakage, 76.1229 • Liver, interventional procedure, 76.1229 • Liver, transplantation, 76.1229, 76.458, 952.76 • Thrombosis, arterial, 952.76
Radiology 1990; 174:1031-1035
1 From the Departments of Radiology (S.B.K., A.B.Z.) and Surgery (B.K.), University of Pittsburgh School of Medicine, Pittsburgh. Received August 23, 1989; revision requested September 30; revision received and accepted November 6. Address reprint requests to A.B.Z., Department of Radiology, Presbyterian-University Hospital, DeSoto at O'Hara Sts, Pittsburgh, PA 15213. 2 Current address: University of Medicine and Dentistry of New Jersey, Newark, NJ. RSNA, 1990
of the most serious complications following liver transplan0 tation is hepatic artery thrombosis NE
(HAT), seen in approximately 8% of transplant recipients (1-3). Ischemia subsequent to HAT usually leads to bile duct necrosis with bile leakage and formation of intrahepatic or hilar bilomas (2). These developments can result in biliary stasis with infection and abscess formation, cholangitis, and sepsis. Retransplantation is often required for patient survival. Percutaneous catheter drainage of infected hepatic bilomas caused by thrombosis of the hepatic artery has been reported as a nonsurgical method of prolonging allograft survival and preventing retransplantation (4,5). In this article, we report our experience with percutaneous drainage of hepatic bilomas in 16 allografts with arterial thrombosis.
PATIENTS AND METHODS The case material is drawn from more than 1,400 liver transplantations performed at our institution over the past 4 years. From these patients, we retrospectively reviewed the case histories and radiologic studies in 22 transplantations complicated by HAT and cholangiographic evidence of intrahepatic biloma formation. Fifteen patients (with 16 hepatic allografts) underwent transhepatic drainage of these bilomas and form the basis of this study (Table). There were 10 children, 0.1-9.6 years of age (mean, 2.6 years), with 11 hepatic allografts, and five adults, 31.3-45.9 years of age (mean, 38.4 years) at transplantation. One child underwent two transplantations, which met our inclusion criteria. Data for both livers are included in this study. Eight patients were male and seven were female. Diagnosis of HAT was made at angiography in 11 cases. In three cases the diagnosis was made at pulsed
Doppler sonography; two of these were confirmed at surgery. One case of an occluded hepatic artery due to an intimal flap was noted at laparotomy performed for presumed bile leak. One patient required ligation of the hepatic artery for treatment of gastrointestinal tract bleeding due to a ruptured pseudoaneurysm of the hepatic artery. In 13 patients (14 allografts), HAT developed within 5-319 days (mean, 53 days) after transplantation. The patient with dissection of the hepatic artery and the patient with pseudoaneurysm rupture followed by surgical ligation had these complications discovered at 622 days and 54 days after transplantation, respectively. Children developed HAT after surgery earlier than adults (children: 563 days, mean = 15 days; adults: 12319 days, mean = 147 days). Intrahepatic fluid collections in central and / or peripheral locations were initially demonstrated by computed tomography (CT) in 15 cases and by T-tube cholangiography in one case. These collections began as either sterile bilomas or as abscesses, but in every case they initially or eventually communicated with the biliary tree. Collections were drained via a percutaneous transhepatic approach with standard interventional radiologic techniques in 14 of 16 cases. In two of these, the catheter was placed into the biloma via the biliary tree rather than by direct placement into the collection. In two cases bilomas formed around previously placed biliary drainage catheters. Both passed through the biliaryenteric anastomosis into the bowel. Catheter sizes ranged from 7 to 8.5 F. All but one patient underwent subsequent catheter exchanges. Two of the cavitary drains were converted to inAbbreviation: HAT = hepatic artery thrombosis.
1031
ternal biliary drains leading into the bowel; four catheters crossed the bile duct confluence to drain both right and left hepatic ducts. RESULTS
Focal low-attenuation areas were seen within the hepatic allograft on CT scans in 15 of the 16 allografts within 81 days (mean, 19 days) of the diagnosis of HAT (Fig 1). These proved to be sterile or infected fluid collections in all cases. Catheter drainage was performed within 0-32 days (mean, 8 days) of CT diagnosis in all but two cases. A catheter cholangiogram enabled diagnosis of a biloma in one patient 54 days after percutaneous transhepatic cholangiography was performed with placement of a biliary drainage catheter into the jejunum. In the other patient, a transhepatic drainage catheter was placed intraoperatively, across a biliary-enteric anastomotic stricture, 6 days before demonstration of a central biloma by means of catheter cholangiography. Eleven patients had central (hilar and parahilar) bilomas, as demonstrated by radiologic studies, that were caused by necrosis of the confluence of the main biliary ducts (Fig 2, Table). Eight patients had bilomas involving the peripheral intrahepatic ducts (Fig 3). Three patients had bilomas in both central and peripheral locations. Of the central bilomas caused by central biliary duct necrosis, two demonstrated little or no communication with the common bile duct or bowel and necessitated retransplantation shortly after drainage was performed. Two patients had central hepatic bilomas that healed with extensive biliary strictures (Fig 4), eventually leading to retransplantation more than 2 years after drainage in one of these patients; the other has maintained his graft for 38 months since drainage. One patient developed a large biliary-portal vein fistula and required a new allograft (Fig 1). One patient had a central biloma that lost communication with the biliary tree. This patient did well for 2 years after drainage. However, internal biliary drainage could not be provided, and he lost large amounts of bile, necessitating retransplantation. Of the remaining five patients with central bilomas, one had extensive necrosis involving the entire biliary tree that necessitated retransplantation (Fig 5). Three had persis1032 • Radiology
Figure 1. Patient 10. Central hepatic biloma. CT scan demonstrates large area of low attenuation within the hilum of the hepatic allograft. The dense structure within the collection represents the internal biliary stent. Presence of large hilar biloma was proved by percutaneous aspiration and catheter drainage. There was extensive necrosis of the central hepatic biliary tree and a fistula extending into the portal vein. Histologic examination of the hepatectomy specimen after retransplantation confirmed these findings and also showed infected bilestained thrombus within the portal veins.
Figure 2. Patient 1. Central hepatic biloma. Catheter cholangiogram demonstrates extensive necrosis of the central biliary tree, including the common hepatic bile duct. The large, irregular central cavity communicates with the intrahepatic biliary tree. There is subhepatic leakage of contrast material, which can be seen draining into a surgically placed sump (arrowheads). Histologic examination of the hepatectomy specimen after retransplantation showed extensive necrosis of the hilar structures, including the main right, left, and common hepatic ducts. (Reprinted, with permission, from reference 6.)
tent sepsis despite drainage, antibiotic coverage, and continued biliary-enteric communication and required retransplantation. One patient had a small central biloma and a separate common hepatic duct stricture. She underwent biliary drainage and balloon dilation of the stricture and still has the original allograft more than 3 years after initial drainage. Seven patients (eight allografts) had peripheral bilomas, three of
Figure 3. Patient 13. Peripheral intrahepatic biloma. Catheter cholangiogram shows necrosis of right hepatic bile ducts and biloma in right hepatic lobe. There is ductal dilatation and irregularity with intraluminal filling defects. There is no evidence of biliary-enteric communication. Note that the cavity communicates with peripheral intrahepatic ducts (arrows). Despite external drainage, the cavity continued to enlarge. Communication with the bowel was never demonstrated. The patient underwent retransplantation 10 weeks after initial drainage. Histologic examination of the hepatectomy specimen after retransplantation showed a biloma cavity in right lobe surrounded by necrotic liver. Multiple necrotic bile ducts were seen containing bile casts and numerous colonies of bacteria. In addition, there were necrosis of hilar structures and strictures of main hepatic bile ducts.
Figure 4. Patient 3. Central biliary strictures after drainage of central biloma. Percutaneous transhepatic cholangiogram demonstrates biliary obstruction due to strictures of multiple bile ducts in the porta hepatis of a 1-year-old child. There is minimal flow into the jejunum. At 1 month of age, this patient underwent successful drainage of a central biloma that subsequently healed with scarring, causing multiple central strictures. Because of strictures involving multiple ducts and the patient's age, transhepatic biliary dilation was not performed. Thirty-eight months after drainage, no catheter is in place. Because of liver failure, retransplantation is pending.
March 1990 • Part 2
Summary of Patient Data and Cholangiographic Findings in Transplant Recipients with Hepatic Bilomas after HAT .
Time
from Time from Time from Time from Age at Transplantation Transplantation Transplantation Drainage to Location to Diagnosis Transplantation to Diagnosis Retransplantation to Drainage of (y) Patient of HAT (d) of Bilonta (d) of Biloma (d) (d) Biloma
7.8
8
622
619
651
21
3.3
11
12
50
0.1
16
10
NA*
9.6 63
44
55
31
0.7
34
36
773
1.3
11
92
101
63
0.7
13
13
13
NA*
13
18
22
770
13
34
36
41
10
22
NA*
16
68
72
18
12
20
21
119
319
324
324
69
213
258
280
79
244
190
NA*
51
39
9at
2.6 0.8
9bt
1.0
Cholangiographic Findings
C
Complete necrosis of central hepatic bile ducts with large hilar biloma and bile leak into peritoneum (Fig 2) Single peripheral.bilonla in right hepatic lobe; stricture of left hepatic duct causing partial obstruction C Central hilar biloma that healed with stricture involving multiple central hepatic bile ducts (Fig 4) C, P Single peripheral bi.loma in right hepatic lobe and complete necrosis of central hepatic bile ducts with large hilar biloma; both bilomas communicated via a right hepatic bile duct C Central biloma extending into left hepatic lobe with bile leak into peritoneum Extensive necrosis of central'heC pati.c ducts with large hi.lar biloma Large biloma in left hepatic lobe; stricture' of common hepatic duct and hepaticojejunostomy successfully treated with balloon dilation (Fig 6) C Findings almost identical to those in patient 3 P Necrosis of central hepatic bile ducts with high-grade biliary obstruction Three peripheral bi.lomas in right hepatic lobe drained with three catheters; cavities resolved and catheters were pulled Complete necrosis of central he C pati,c bile ducts with large central biloma and fistula toportal vein (Fig 1) C Complete necrosis of central hepatic bile ducts to the choledochocholedochostomy anastomosis with large hilar biloma C, P Extensive necrosis of the entire allograft biliary tree to the choledochoclioledochostomy anastomosis, and large bilomas in right and left hepatic lobe; multiple intraluminal filling defects due to necrotic debris within ducts (Fig 5) Peripheral biloma in right hepatic P lobe that continued to enlarfe . despite drainage; necrosis o multiple right hepatic ducts; complete biliary obstruction with no flow into bowel; intraluminal filling defects due to necrotic debris within ducts (Fig 3) C Small biloma at confluence of fight and left hepatic ducts; stricture of common hepatic duct successfully treated with balloon dilation P Large peripheral biloma in right hepatic lobe and severe stricture of right hepatic bile duct ,
10
1.1
11
41.6
12
31.3
13
45.9
14
38.4
15
34.8
46
-
Note.—C = central, P = peripheral, NA = not applicable.
* Patients 3, 7, 9 14 still living without retransplantation at 38, 44, 30, and 37 months, respectively, following drainage. I Patient 9 received two hepatic allografts. Data from both are included here. :
which were accompanied by central bilomas. Two of the five patients with only peripheral bilomas demonstrated resolution of the biloma with drainage and have not required new livers (Fig 6). Of the remaining three patients, two had peripheral bilomas Volume 174 • Number 3 • Part 2
that did not resolve after drainage (Fig 3); both have required new livers. One patient received a second transplant because of sepsis 3 days after drainage of a large peripheral biloma and underwent no further radiologic studies.
DISCUSSION
HAT is a devastating complication of liver transplantation that occurs in approximately 8% of liver recipients (1-3). HAT is two to three times more common in children than adults, a Radiology • 1033
fact possibly related to the smaller caliber of both recipient and donor vessels and arterial grafts used in children (1). Children younger than 1 year of age have an even higher prevalence of HAT; one study (1) reported a frequency of 35%. Other factors associated with a higher frequency of HAT include elevated hematocrit (7), retransplantation (1), rejection (8,9-11), anastomotic irregularity (9), infection (8), and unrecognized intimal flap (8). In the liver allograft, the vascular supply to the intrahepatic biliary system is derived from the hepatic artery (3,11,12). Native hepatopetal arterial collaterals are severed at recipient hepatectomy. The portal venous system does provide flow to the liver, but not a significant amount to the biliary tree. Therefore, occlusion of the allograft arterial supply is most likely to cause ischemic necrosis of the biliary tree, often with hepatic infarcts as well (2,13,14). Biliary leakage, manifested as either small isolated hepatic collections or as larger bile-filled areas of hepatic infarction, occurs and usually is followed by infection of the static bile, abscess formation, cholangitis, and bacteremia. Most (94%) of our patients were initially evaluated with CT, which demonstrated homogeneous low-attenuation areas in the central and /or more peripheral areas of the liver (Figs 1, 6a). These were thought to be intrahepatic infarcts, abscesses, or bilomas. Such lesions are most frequently seen in patients with HAT (15,16). The diagnosis of HAT was confirmed at angiography or laparotomy in all but one patient. In this patient, HAT was diagnosed at duplex sonography. Percutaneous drainage of hepatic bilomas in liver transplants with HAT has been reported previously (4,5,17). An earlier report from our institution described five patients who developed bilomas that were drained percutaneously (17). Four of these required retransplantation. A recent report by Rollins et al (5) details their experience with biloma drainage in two pediatric patients. One required retransplantation 21 weeks after initial transplantation, and one has done well for 8 months without retransplantation. The bilomas in these two patients are described as cavities involving the peripheral bile ducts. Hoffer et al (4) recently published a report about a series of three pediatric patients with bilomas who have survived without retransplantation 1-4 years after per1034 • Radiology
a.
Figure 5. Patient 12. Necrosis of the entire allograft biliary tree. Sinogram 6 weeks after percutaneous drainage of bilomas in right and left hepatic lobes (straight arrows) shows communication with a necrotic biliary tree. Generalized ductal irregularity and dilatation with diffuse intraluminal filling defects are seen. Note hilar biloma cavity (small arrowheads) that replaces donor common duct. Recipient common bile duct (curved arrow) below choledochocholedochostomy anastomosis (large arrowhead) is normal. Histologic examination of the hepatectomy specimen after retransplantation showed extensive bile duct necrosis with purulent and necrotic material filling the entire donor biliary tree. (Reprinted, with permission, from reference 2.)
cutaneous drainage. The appearance and location of these bilomas are not described, except for one illustrated case in which the biloma seemed to be single and peripheral. Most of the bilomas in our series were central and involved necrosis of the main biliary ducts (Figs 2, 5). From our study, it appears that the outcome of most of these allografts will be poor. The bilomas that we can demonstrate and drain by means of CT and fluoroscopy are complications of HAT rather than primary diseases that can be completely cured by drainage. Most of our patients demonstrated extensive biliary necrosis due to HAT. In addition, most of these livers have multiple bilomas or abscesses, many of which are too small for us to image. Most patients who needed retransplantation needed it because of sepsis and cholangitis that was not treatable with conventional antibiotics and drainage. Varying degrees of hepatic and biliary necrosis were noted at pathologic examination of all allograft hepatectomy specimens. In six of our patients, biloma drainage has provided long-term palliation of hepatic sepsis. Four of these patients have lived 30-44 months without requiring new livers; two of the four had small central bilomas that maintained communication with
•
c. Figure 6. Patient 7. Peripheral intrahepatic biloma. (a) CT scan shows large low-attenuation lesion in left hepatic lobe of an 8month-old patient 2 weeks after transplantation. (b) One week after drainage, injection of contrast material through catheter shows the cavity communicates with a right hepatic bile duct. (c) CT scan shows almost complete resolution of the cavity 6 weeks after drainage. The catheter was removed shortly thereafter. This patient also had a biliary stricture at the confluence of the right and left hepatic ducts, successfully treated with balloon dilation. She is currently doing well 3 years after transplantation.
the bowel, and two patients had one or more peripheral bilomas that resolved completely with drainage. Two other patients did well for longer than 2 years before they needed retransplantation; one of these had a small central biloma that healed with strictures involving multiple right and left hepatic ducts and thereby lost adequate biliary-enteric communication. The other patient had a biloma that lost communication with the proximal biliary tree and bowel. March 1990 • Part 2
As long as the catheter remained open to external drainage, he did well. However, internal biliary drainage could not be provided and he lost large amounts of bile. Ultimately, therefore, retransplantation was needed. Five of the six patients in whom long-term palliation was achieved by means of percutaneous biloma drainage are children. We have previously reported that collateral arterial growth into the allograft liver occurs early in children (15). In fact, we are unaware of any report of angiographically demonstrated arterial collaterals after HAT in adult hepatic allografts. This difference in collateral development may be partially responsible for the success in maintaining these grafts by means of drainage in children (2,3,15). We have observed the formation of nonanastomotic biliary strictures at the site of bile duct necrosis in two of our patients (Fig 4), presumably due to healing and fibrous scarring of the ducts. In other patients, nonanastomotic strictures following HAT have occurred primarily without previous bilomas (2); such strictures occurred in one of our patients. Biliary obstruction has been demonstrated proximal to the strictures. Biliary drainage and balloon dilation of the stricture is a useful method of further preserving hepatic function in this group of patients. In summary, biloma drainage in liver transplant recipients who have suffered HAT can prolong allograft survival and prevent retransplanta-
Volume 174 • Number 3 • Part 2
tion in a few cases. These would include cases of small bilomas that are peripheral and resolve completely on drainage and small central bilomas that resolve and maintain their biliary-enteric communication after drainage. Patients who have cholangiographic evidence of extensive bile duct necrosis will eventually need retransplantation. In these patients drainage is useful in the initial treatment of biliary sepsis, providing time in which to find a suitable donor liver. n Acknowledgment: We thank Terri Chuba for manuscript preparation.
References 1. Todo S, Makowka L, Tzakis AG, et al. Hepatic artery in liver transplantation. Transplant Proc 1987; 19:2406-2411. 2. Zajko AB, Campbell WL, Logsdon GA, et al. Cholangiographic findings in hepatic artery occlusion after liver transplantation. AIR 1987; 149:485-489. 3. Tzakis AG, Gordon RD, Shaw BW Jr, Iwatsuki S, Starzl TE. Clinical presentation of hepatic artery thrombosis after liver transplantation in the cyclosporine era. Transplantation 1985; 40:667-671. 4. Hoffer FA, Teele RL, Lillehei CW, Vacanti JP. Infected bilomas and hepatic artery thrombosis in infant recipients of liver transplants: interventional radiology and medical therapy as an alternative to retransplantation. Radiology 1988; 169:435438. 5. Rollins NK, Andrews WS, Currarino G, Miller RH, Smith TH, Redman HC. Infected bile lakes following pediatric liver transplantation: nonsurgical management. Radiology 1988; 166:169-171. 6. Zajko AB, Campbell WL, Logsdon GA, et al. Biliary complications in liver allografts after hepatic artery occlusion: a 6 1/2 year study. Transplant Proc 1988; 20:607609.
7. Tisone G, Gunson BK, Buckels JAC, McMaster P. Raised hematocrit: a contributing factor to hepatic artery thrombosis following liver transplantation. Transplantation 1988; 46:162-163. 8. Esquivel CO, Koneru B, Karrer FM, et al. Liver transplantation before 1 year of age. J Pediatr 1987; 110:545-548. 9. White RM, Zajko AB, Demetris AJ, Bron KM, Dekker A, Starzl TE. Liver transplant rejection: angiographic findings in 35 patients. AJR 1987; 148:1095-1098. 10. Demetris AJ, Lasky S, Van Thiel DH, Starzl TE, Dekker A. Pathology of hepatic transplantation: a review of 62 adult allograft recipients immunosuppressed with a cyclosporine /steroid regimen. Am J Pathol 1985; 118:151-161. 11. Demetris AJ, Jaffe R, Starzl TE. A review of adult and pediatric post-transplant liver pathology. II. Pathol Annu 1987; 22:347-386. 12. Rappaport AM. Physioanatomic considerations. In: Schiff L, Schiff ER, eds. Diseases of the liver. 6th ed. Philadelphia: Lippincott, 1987; 1-46. 13. Seely TT, Blumenfeld CM, Ikeda R, Knapp W, Ruebner BH. Hepatic infarction. Hum Pathol 1972; 3:265-276. 14. Loeffler L. Factors determining necrosis or survival of liver tissue after ligation of hepatic artery. Arch Pathol 1936; 21:496503. 15. Wozney P, Zajko AB, Bron KM, Point S, Starzl TE. Vascular complications after liver transplantation: a 5-year experience. AJR 1986; 147:657-663. 16. Segel MC, Zajko AB, Bowen A, et al. Hepatic artery thrombosis after liver transplantation: radiologic evaluation. AIR 1986; 146:137-141. 17. Zajko AB, Bron KM, Campbell WL, Behal R, Van Thiel DH, Starzl TE. Percutaneous transhepatic cholangiography and biliary drainage after liver transplantation: a five-year experience. Gastrointest Radiol 1987; 12:137-143.
Radiology • 1035
Hepatic Bilomas Due to Hepatic Artery Thrombosis in Liver Transplant Recipients: Percutaneous Drainage and Clinical Outcome' During the past 4 years, the authors performed catheter drainage in 15 patients (five adults and 10 children) with 16 hepatic allografts who had intrahepatic bilomas after occlusion of the hepatic artery. Ten of the 16 (62%) allografts (in four adults and six children) were replaced within 4 months of drainage: Nine were replaced because of biliary sepsis or abscess, and one was replaced because of the absence of biliary-enteric communication. Most of these patients had cholangiographic evidence of extensive bile duct necrosis. In two patients, retransplantation was avoided for longer than 2 years. One of these needed a new liver because of multiple central biliary strictures. Four patients have now lived for 30-44 months since initiation of drainage without needing new livers. Despite drainage, the outcome of most of these allografts has been poor. However, in some liver transplant recipients who have had hepatic artery thrombosis, biloma drainage can prolong allograft survival and prevent retransplantation. Index terms: Bile ducts, interventional procedure, 76.1229 • Bile ducts, leakage, 76.1229 • Liver, interventional procedure, 76.1229 • Liver, transplantation, 76.1229, 76.458, 952.76 • Thrombosis, arterial, 952.76
Radiology 1990; 174:1031-1035
1 From the Departments of Radiology (S.B.K., A.B.Z.) and Surgery (B.K.), University of Pittsburgh School of Medicine, Pittsburgh. Received August 23, 1989; revision requested September 30; revision received and accepted November 6. Address reprint requests to A.B.Z., Department of Radiology, Presbyterian-University Hospital, DeSoto at O'Hara Sts, Pittsburgh, PA 15213. 2 Current address: University of Medicine and Dentistry of New Jersey, Newark, NJ. RSNA, 1990
of the most serious complications following liver transplan0 tation is hepatic artery thrombosis NE
(HAT), seen in approximately 8% of transplant recipients (1-3). Ischemia subsequent to HAT usually leads to bile duct necrosis with bile leakage and formation of intrahepatic or hilar bilomas (2). These developments can result in biliary stasis with infection and abscess formation, cholangitis, and sepsis. Retransplantation is often required for patient survival. Percutaneous catheter drainage of infected hepatic bilomas caused by thrombosis of the hepatic artery has been reported as a nonsurgical method of prolonging allograft survival and preventing retransplantation (4,5). In this article, we report our experience with percutaneous drainage of hepatic bilomas in 16 allografts with arterial thrombosis.
PATIENTS AND METHODS The case material is drawn from more than 1,400 liver transplantations performed at our institution over the past 4 years. From these patients, we retrospectively reviewed the case histories and radiologic studies in 22 transplantations complicated by HAT and cholangiographic evidence of intrahepatic biloma formation. Fifteen patients (with 16 hepatic allografts) underwent transhepatic drainage of these bilomas and form the basis of this study (Table). There were 10 children, 0.1-9.6 years of age (mean, 2.6 years), with 11 hepatic allografts, and five adults, 31.3-45.9 years of age (mean, 38.4 years) at transplantation. One child underwent two transplantations, which met our inclusion criteria. Data for both livers are included in this study. Eight patients were male and seven were female. Diagnosis of HAT was made at angiography in 11 cases. In three cases the diagnosis was made at pulsed
Doppler sonography; two of these were confirmed at surgery. One case of an occluded hepatic artery due to an intimal flap was noted at laparotomy performed for presumed bile leak. One patient required ligation of the hepatic artery for treatment of gastrointestinal tract bleeding due to a ruptured pseudoaneurysm of the hepatic artery. In 13 patients (14 allografts), HAT developed within 5-319 days (mean, 53 days) after transplantation. The patient with dissection of the hepatic artery and the patient with pseudoaneurysm rupture followed by surgical ligation had these complications discovered at 622 days and 54 days after transplantation, respectively. Children developed HAT after surgery earlier than adults (children: 563 days, mean = 15 days; adults: 12319 days, mean = 147 days). Intrahepatic fluid collections in central and / or peripheral locations were initially demonstrated by computed tomography (CT) in 15 cases and by T-tube cholangiography in one case. These collections began as either sterile bilomas or as abscesses, but in every case they initially or eventually communicated with the biliary tree. Collections were drained via a percutaneous transhepatic approach with standard interventional radiologic techniques in 14 of 16 cases. In two of these, the catheter was placed into the biloma via the biliary tree rather than by direct placement into the collection. In two cases bilomas formed around previously placed biliary drainage catheters. Both passed through the biliaryenteric anastomosis into the bowel. Catheter sizes ranged from 7 to 8.5 F. All but one patient underwent subsequent catheter exchanges. Two of the cavitary drains were converted to inAbbreviation: HAT = hepatic artery thrombosis.
1031
ternal biliary drains leading into the bowel; four catheters crossed the bile duct confluence to drain both right and left hepatic ducts. RESULTS
Focal low-attenuation areas were seen within the hepatic allograft on CT scans in 15 of the 16 allografts within 81 days (mean, 19 days) of the diagnosis of HAT (Fig 1). These proved to be sterile or infected fluid collections in all cases. Catheter drainage was performed within 0-32 days (mean, 8 days) of CT diagnosis in all but two cases. A catheter cholangiogram enabled diagnosis of a biloma in one patient 54 days after percutaneous transhepatic cholangiography was performed with placement of a biliary drainage catheter into the jejunum. In the other patient, a transhepatic drainage catheter was placed intraoperatively, across a biliary-enteric anastomotic stricture, 6 days before demonstration of a central biloma by means of catheter cholangiography. Eleven patients had central (hilar and parahilar) bilomas, as demonstrated by radiologic studies, that were caused by necrosis of the confluence of the main biliary ducts (Fig 2, Table). Eight patients had bilomas involving the peripheral intrahepatic ducts (Fig 3). Three patients had bilomas in both central and peripheral locations. Of the central bilomas caused by central biliary duct necrosis, two demonstrated little or no communication with the common bile duct or bowel and necessitated retransplantation shortly after drainage was performed. Two patients had central hepatic bilomas that healed with extensive biliary strictures (Fig 4), eventually leading to retransplantation more than 2 years after drainage in one of these patients; the other has maintained his graft for 38 months since drainage. One patient developed a large biliary-portal vein fistula and required a new allograft (Fig 1). One patient had a central biloma that lost communication with the biliary tree. This patient did well for 2 years after drainage. However, internal biliary drainage could not be provided, and he lost large amounts of bile, necessitating retransplantation. Of the remaining five patients with central bilomas, one had extensive necrosis involving the entire biliary tree that necessitated retransplantation (Fig 5). Three had persis1032 • Radiology
Figure 1. Patient 10. Central hepatic biloma. CT scan demonstrates large area of low attenuation within the hilum of the hepatic allograft. The dense structure within the collection represents the internal biliary stent. Presence of large hilar biloma was proved by percutaneous aspiration and catheter drainage. There was extensive necrosis of the central hepatic biliary tree and a fistula extending into the portal vein. Histologic examination of the hepatectomy specimen after retransplantation confirmed these findings and also showed infected bilestained thrombus within the portal veins.
Figure 2. Patient 1. Central hepatic biloma. Catheter cholangiogram demonstrates extensive necrosis of the central biliary tree, including the common hepatic bile duct. The large, irregular central cavity communicates with the intrahepatic biliary tree. There is subhepatic leakage of contrast material, which can be seen draining into a surgically placed sump (arrowheads). Histologic examination of the hepatectomy specimen after retransplantation showed extensive necrosis of the hilar structures, including the main right, left, and common hepatic ducts. (Reprinted, with permission, from reference 6.)
tent sepsis despite drainage, antibiotic coverage, and continued biliary-enteric communication and required retransplantation. One patient had a small central biloma and a separate common hepatic duct stricture. She underwent biliary drainage and balloon dilation of the stricture and still has the original allograft more than 3 years after initial drainage. Seven patients (eight allografts) had peripheral bilomas, three of
Figure 3. Patient 13. Peripheral intrahepatic biloma. Catheter cholangiogram shows necrosis of right hepatic bile ducts and biloma in right hepatic lobe. There is ductal dilatation and irregularity with intraluminal filling defects. There is no evidence of biliary-enteric communication. Note that the cavity communicates with peripheral intrahepatic ducts (arrows). Despite external drainage, the cavity continued to enlarge. Communication with the bowel was never demonstrated. The patient underwent retransplantation 10 weeks after initial drainage. Histologic examination of the hepatectomy specimen after retransplantation showed a biloma cavity in right lobe surrounded by necrotic liver. Multiple necrotic bile ducts were seen containing bile casts and numerous colonies of bacteria. In addition, there were necrosis of hilar structures and strictures of main hepatic bile ducts.
Figure 4. Patient 3. Central biliary strictures after drainage of central biloma. Percutaneous transhepatic cholangiogram demonstrates biliary obstruction due to strictures of multiple bile ducts in the porta hepatis of a 1-year-old child. There is minimal flow into the jejunum. At 1 month of age, this patient underwent successful drainage of a central biloma that subsequently healed with scarring, causing multiple central strictures. Because of strictures involving multiple ducts and the patient's age, transhepatic biliary dilation was not performed. Thirty-eight months after drainage, no catheter is in place. Because of liver failure, retransplantation is pending.
March 1990 • Part 2
Summary of Patient Data and Cholangiographic Findings in Transplant Recipients with Hepatic Bilomas after HAT .
Time
from Time from Time from Time from Age at Transplantation Transplantation Transplantation Drainage to Location to Diagnosis Transplantation to Diagnosis Retransplantation to Drainage of (y) Patient of HAT (d) of Bilonta (d) of Biloma (d) (d) Biloma
7.8
8
622
619
651
21
3.3
11
12
50
0.1
16
10
NA*
9.6 63
44
55
31
0.7
34
36
773
1.3
11
92
101
63
0.7
13
13
13
NA*
13
18
22
770
13
34
36
41
10
22
NA*
16
68
72
18
12
20
21
119
319
324
324
69
213
258
280
79
244
190
NA*
51
39
9at
2.6 0.8
9bt
1.0
Cholangiographic Findings
C
Complete necrosis of central hepatic bile ducts with large hilar biloma and bile leak into peritoneum (Fig 2) Single peripheral.bilonla in right hepatic lobe; stricture of left hepatic duct causing partial obstruction C Central hilar biloma that healed with stricture involving multiple central hepatic bile ducts (Fig 4) C, P Single peripheral bi.loma in right hepatic lobe and complete necrosis of central hepatic bile ducts with large hilar biloma; both bilomas communicated via a right hepatic bile duct C Central biloma extending into left hepatic lobe with bile leak into peritoneum Extensive necrosis of central'heC pati.c ducts with large hi.lar biloma Large biloma in left hepatic lobe; stricture' of common hepatic duct and hepaticojejunostomy successfully treated with balloon dilation (Fig 6) C Findings almost identical to those in patient 3 P Necrosis of central hepatic bile ducts with high-grade biliary obstruction Three peripheral bi.lomas in right hepatic lobe drained with three catheters; cavities resolved and catheters were pulled Complete necrosis of central he C pati,c bile ducts with large central biloma and fistula toportal vein (Fig 1) C Complete necrosis of central hepatic bile ducts to the choledochocholedochostomy anastomosis with large hilar biloma C, P Extensive necrosis of the entire allograft biliary tree to the choledochoclioledochostomy anastomosis, and large bilomas in right and left hepatic lobe; multiple intraluminal filling defects due to necrotic debris within ducts (Fig 5) Peripheral biloma in right hepatic P lobe that continued to enlarfe . despite drainage; necrosis o multiple right hepatic ducts; complete biliary obstruction with no flow into bowel; intraluminal filling defects due to necrotic debris within ducts (Fig 3) C Small biloma at confluence of fight and left hepatic ducts; stricture of common hepatic duct successfully treated with balloon dilation P Large peripheral biloma in right hepatic lobe and severe stricture of right hepatic bile duct ,
10
1.1
11
41.6
12
31.3
13
45.9
14
38.4
15
34.8
46
-
Note.—C = central, P = peripheral, NA = not applicable.
* Patients 3, 7, 9 14 still living without retransplantation at 38, 44, 30, and 37 months, respectively, following drainage. I Patient 9 received two hepatic allografts. Data from both are included here. :
which were accompanied by central bilomas. Two of the five patients with only peripheral bilomas demonstrated resolution of the biloma with drainage and have not required new livers (Fig 6). Of the remaining three patients, two had peripheral bilomas Volume 174 • Number 3 • Part 2
that did not resolve after drainage (Fig 3); both have required new livers. One patient received a second transplant because of sepsis 3 days after drainage of a large peripheral biloma and underwent no further radiologic studies.
DISCUSSION
HAT is a devastating complication of liver transplantation that occurs in approximately 8% of liver recipients (1-3). HAT is two to three times more common in children than adults, a Radiology • 1033
fact possibly related to the smaller caliber of both recipient and donor vessels and arterial grafts used in children (1). Children younger than 1 year of age have an even higher prevalence of HAT; one study (1) reported a frequency of 35%. Other factors associated with a higher frequency of HAT include elevated hematocrit (7), retransplantation (1), rejection (8,9-11), anastomotic irregularity (9), infection (8), and unrecognized intimal flap (8). In the liver allograft, the vascular supply to the intrahepatic biliary system is derived from the hepatic artery (3,11,12). Native hepatopetal arterial collaterals are severed at recipient hepatectomy. The portal venous system does provide flow to the liver, but not a significant amount to the biliary tree. Therefore, occlusion of the allograft arterial supply is most likely to cause ischemic necrosis of the biliary tree, often with hepatic infarcts as well (2,13,14). Biliary leakage, manifested as either small isolated hepatic collections or as larger bile-filled areas of hepatic infarction, occurs and usually is followed by infection of the static bile, abscess formation, cholangitis, and bacteremia. Most (94%) of our patients were initially evaluated with CT, which demonstrated homogeneous low-attenuation areas in the central and /or more peripheral areas of the liver (Figs 1, 6a). These were thought to be intrahepatic infarcts, abscesses, or bilomas. Such lesions are most frequently seen in patients with HAT (15,16). The diagnosis of HAT was confirmed at angiography or laparotomy in all but one patient. In this patient, HAT was diagnosed at duplex sonography. Percutaneous drainage of hepatic bilomas in liver transplants with HAT has been reported previously (4,5,17). An earlier report from our institution described five patients who developed bilomas that were drained percutaneously (17). Four of these required retransplantation. A recent report by Rollins et al (5) details their experience with biloma drainage in two pediatric patients. One required retransplantation 21 weeks after initial transplantation, and one has done well for 8 months without retransplantation. The bilomas in these two patients are described as cavities involving the peripheral bile ducts. Hoffer et al (4) recently published a report about a series of three pediatric patients with bilomas who have survived without retransplantation 1-4 years after per1034 • Radiology
a.
Figure 5. Patient 12. Necrosis of the entire allograft biliary tree. Sinogram 6 weeks after percutaneous drainage of bilomas in right and left hepatic lobes (straight arrows) shows communication with a necrotic biliary tree. Generalized ductal irregularity and dilatation with diffuse intraluminal filling defects are seen. Note hilar biloma cavity (small arrowheads) that replaces donor common duct. Recipient common bile duct (curved arrow) below choledochocholedochostomy anastomosis (large arrowhead) is normal. Histologic examination of the hepatectomy specimen after retransplantation showed extensive bile duct necrosis with purulent and necrotic material filling the entire donor biliary tree. (Reprinted, with permission, from reference 2.)
cutaneous drainage. The appearance and location of these bilomas are not described, except for one illustrated case in which the biloma seemed to be single and peripheral. Most of the bilomas in our series were central and involved necrosis of the main biliary ducts (Figs 2, 5). From our study, it appears that the outcome of most of these allografts will be poor. The bilomas that we can demonstrate and drain by means of CT and fluoroscopy are complications of HAT rather than primary diseases that can be completely cured by drainage. Most of our patients demonstrated extensive biliary necrosis due to HAT. In addition, most of these livers have multiple bilomas or abscesses, many of which are too small for us to image. Most patients who needed retransplantation needed it because of sepsis and cholangitis that was not treatable with conventional antibiotics and drainage. Varying degrees of hepatic and biliary necrosis were noted at pathologic examination of all allograft hepatectomy specimens. In six of our patients, biloma drainage has provided long-term palliation of hepatic sepsis. Four of these patients have lived 30-44 months without requiring new livers; two of the four had small central bilomas that maintained communication with
•
c. Figure 6. Patient 7. Peripheral intrahepatic biloma. (a) CT scan shows large low-attenuation lesion in left hepatic lobe of an 8month-old patient 2 weeks after transplantation. (b) One week after drainage, injection of contrast material through catheter shows the cavity communicates with a right hepatic bile duct. (c) CT scan shows almost complete resolution of the cavity 6 weeks after drainage. The catheter was removed shortly thereafter. This patient also had a biliary stricture at the confluence of the right and left hepatic ducts, successfully treated with balloon dilation. She is currently doing well 3 years after transplantation.
the bowel, and two patients had one or more peripheral bilomas that resolved completely with drainage. Two other patients did well for longer than 2 years before they needed retransplantation; one of these had a small central biloma that healed with strictures involving multiple right and left hepatic ducts and thereby lost adequate biliary-enteric communication. The other patient had a biloma that lost communication with the proximal biliary tree and bowel. March 1990 • Part 2
As long as the catheter remained open to external drainage, he did well. However, internal biliary drainage could not be provided and he lost large amounts of bile. Ultimately, therefore, retransplantation was needed. Five of the six patients in whom long-term palliation was achieved by means of percutaneous biloma drainage are children. We have previously reported that collateral arterial growth into the allograft liver occurs early in children (15). In fact, we are unaware of any report of angiographically demonstrated arterial collaterals after HAT in adult hepatic allografts. This difference in collateral development may be partially responsible for the success in maintaining these grafts by means of drainage in children (2,3,15). We have observed the formation of nonanastomotic biliary strictures at the site of bile duct necrosis in two of our patients (Fig 4), presumably due to healing and fibrous scarring of the ducts. In other patients, nonanastomotic strictures following HAT have occurred primarily without previous bilomas (2); such strictures occurred in one of our patients. Biliary obstruction has been demonstrated proximal to the strictures. Biliary drainage and balloon dilation of the stricture is a useful method of further preserving hepatic function in this group of patients. In summary, biloma drainage in liver transplant recipients who have suffered HAT can prolong allograft survival and prevent retransplanta-
Volume 174 • Number 3 • Part 2
tion in a few cases. These would include cases of small bilomas that are peripheral and resolve completely on drainage and small central bilomas that resolve and maintain their biliary-enteric communication after drainage. Patients who have cholangiographic evidence of extensive bile duct necrosis will eventually need retransplantation. In these patients drainage is useful in the initial treatment of biliary sepsis, providing time in which to find a suitable donor liver. n Acknowledgment: We thank Terri Chuba for manuscript preparation.
References 1. Todo S, Makowka L, Tzakis AG, et al. Hepatic artery in liver transplantation. Transplant Proc 1987; 19:2406-2411. 2. Zajko AB, Campbell WL, Logsdon GA, et al. Cholangiographic findings in hepatic artery occlusion after liver transplantation. AIR 1987; 149:485-489. 3. Tzakis AG, Gordon RD, Shaw BW Jr, Iwatsuki S, Starzl TE. Clinical presentation of hepatic artery thrombosis after liver transplantation in the cyclosporine era. Transplantation 1985; 40:667-671. 4. Hoffer FA, Teele RL, Lillehei CW, Vacanti JP. Infected bilomas and hepatic artery thrombosis in infant recipients of liver transplants: interventional radiology and medical therapy as an alternative to retransplantation. Radiology 1988; 169:435438. 5. Rollins NK, Andrews WS, Currarino G, Miller RH, Smith TH, Redman HC. Infected bile lakes following pediatric liver transplantation: nonsurgical management. Radiology 1988; 166:169-171. 6. Zajko AB, Campbell WL, Logsdon GA, et al. Biliary complications in liver allografts after hepatic artery occlusion: a 6 1/2 year study. Transplant Proc 1988; 20:607609.
7. Tisone G, Gunson BK, Buckels JAC, McMaster P. Raised hematocrit: a contributing factor to hepatic artery thrombosis following liver transplantation. Transplantation 1988; 46:162-163. 8. Esquivel CO, Koneru B, Karrer FM, et al. Liver transplantation before 1 year of age. J Pediatr 1987; 110:545-548. 9. White RM, Zajko AB, Demetris AJ, Bron KM, Dekker A, Starzl TE. Liver transplant rejection: angiographic findings in 35 patients. AJR 1987; 148:1095-1098. 10. Demetris AJ, Lasky S, Van Thiel DH, Starzl TE, Dekker A. Pathology of hepatic transplantation: a review of 62 adult allograft recipients immunosuppressed with a cyclosporine /steroid regimen. Am J Pathol 1985; 118:151-161. 11. Demetris AJ, Jaffe R, Starzl TE. A review of adult and pediatric post-transplant liver pathology. II. Pathol Annu 1987; 22:347-386. 12. Rappaport AM. Physioanatomic considerations. In: Schiff L, Schiff ER, eds. Diseases of the liver. 6th ed. Philadelphia: Lippincott, 1987; 1-46. 13. Seely TT, Blumenfeld CM, Ikeda R, Knapp W, Ruebner BH. Hepatic infarction. Hum Pathol 1972; 3:265-276. 14. Loeffler L. Factors determining necrosis or survival of liver tissue after ligation of hepatic artery. Arch Pathol 1936; 21:496503. 15. Wozney P, Zajko AB, Bron KM, Point S, Starzl TE. Vascular complications after liver transplantation: a 5-year experience. AJR 1986; 147:657-663. 16. Segel MC, Zajko AB, Bowen A, et al. Hepatic artery thrombosis after liver transplantation: radiologic evaluation. AIR 1986; 146:137-141. 17. Zajko AB, Bron KM, Campbell WL, Behal R, Van Thiel DH, Starzl TE. Percutaneous transhepatic cholangiography and biliary drainage after liver transplantation: a five-year experience. Gastrointest Radiol 1987; 12:137-143.
Radiology • 1035
