Early Detection of a Hepatic Artery Pseudoaneurysm After Liver Transplantation Is the Determinant of Survival

Early Detection of a Hepatic Artery Pseudoaneurysm After Liver Transplantation Is the Determinant of Survival K.-S. Jenga,*, C.-C. Huangb, C.-K. Linc, C.-C. Linc, C.-C. Liangc, C.-S. Chungc, M.-T. Wengc, and K.-H. Chena a Department of Surgery, bDepartment of Radiology, and cDivision of HepatoGastroenterology, Far Eastern Memorial Hospital, Taipei, Taiwan

ABSTRACT Background. Hepatic artery pseudoaneurysm (PA) after liver transplantation (LT) is a rare but potentially fatal complication. Among a series of 50 patients of LT, we experienced 3 such cases. Some authors also have reported cases of PA, either intrahepatic or extrahepatic. The aim of this study was to investigate the important factors that affect the treatment outcome. Methods. Three patients were presented. To analyze the factors, not only our patients but also the patients with PA reported in the literature (including 10 case series and 23 case reports) were enrolled for analysis. The possible factors probably affecting the survival were compared statistically, including age, sex, clinical manifestation as bleeding (including gastrointestinal bleeding, hemobilia, or intra-abdominal bleeding), treatment (with embolization or surgical exploration or stent), diagnosis establishment before or after bleeding, and so forth. Results. From univariate analysis, the significant factors that affect survival are sex (female) (P ¼ .036), stent treatment (P ¼ .006), and early detection (P ¼ .036), whereas age (P ¼ .493) and presentation with hemorrhage (P ¼ .877) are not significant factors. However, according to multivariate analysis, stent treatment has a borderline significance (P ¼ .056). Conclusions. Early detection of such a life-threatening complication is a key determinant of survival. “Early” does not refer to early postoperative days but means the detection prior to the rupture of the pseudoaneurysm. Postoperative imaging studies such as computed tomographic scan or magnetic resonance cholangiopancreatography early and periodically to follow up the graft status is recommended, especially for those who had received other interventions before or after the liver transplantation.

H

EPATIC artery pseudoaneurysm (PA) after liver transplantation (LT) is a rare but devastating and often fatal complication [1e26]. Among a series of 50 patients of LT, we experienced 3 such cases. Some authors have also reported cases with PA of the hepatic artery after LT, either intrahepatic or extrahepatic. The aim of the present study was to investigate the important factors that affect the survival. METHODS After providing written informed consent, 50 patients who received LT (including cadaver donor and living related donor) at our

institution since January 2011 to December 2014 were enrolled into the study. Institutional internal review board approval was obtained (Table 1). Before liver transplantation, to assess the variation of vessels and biliary system, both tri-phase computed tomographic (CT) scan of liver and magnetic resonance cholangiopancreatography (MRCP) were routinely performed for each recipient and each living donor

*Address correspondence to Kuo-Shyang Jeng, Department of Surgery, Far Eastern Memorial Hospital, No. 21, Section 2, Nanya S. Road, Banciao District, New Taipei City 220, Taiwan, R.O.C. E-mail: [email protected]

ª 2016 Elsevier Inc. All rights reserved. 360 Park Avenue South, New York, NY 10010-1710

0041-1345/16 http://dx.doi.org/10.1016/j.transproceed.2015.11.017

Transplantation Proceedings, 48, 1149e1155 (2016)

1149

After

Before

147

762 55 3‡

M

63 2†

M

Treatment Imaging Studies

44 1*

Possible predisposing factor. Abbreviations: HBV, hepatitis B viral infection; HCC, hepatocellular carcinoma; CT, computed tomographic scan; MRCP, magnetic resonance cholangopan creato graphy; TAE, transcatheter hepatic arterical embolization; ERBD, endoscopicretrograde biliary stent; PTBD, percutaneous transhepatic biliary drcuin age. *Dislodgement of bile duct stent (ERBD stent) for bile duct stenosis, PTBD insertion, hemobilia on the second day after PTBD. † ERBD stent for bile leak after transplantation, bleeding 4 months later. ‡ Mild stenosis at hepatic artery anastomosis, PTBD placement.

After 38

Alcoholic liver cirrhosis Deceased Branch of Rt hepatic Hypovolemic shock artery, extrahepatic after hemobilia HBV carrier, Living Hepatic artery near Hypovolemic shock liver cirrhosis, HCC anastomosis, extrahepatic after internal bleeding HBV carrier, Living Hepatic artery, intrahepatic Jaundice, fatigue liver cirrhosis, HCC

Detection Before or After Bleeding Interval (Days) Clinical Presentation Location of PA

Table 1. Summary of Our Patients With Hepatic Artery Pseudoaneurysm (PA) After Liver Transplantation

Types of Donor Cause of LT No

Sex Patient Age (yr)

M

Outcome

JENG, HUANG, LIN ET AL CT, arteriography TAE failed, Died exploration CT, arteriography TAE failed, Died exploration CT, MRCP, Vascular stent for Survived arteriography exclusion of PA

1150

as our routine. However, for some cadaver donors, because of the severe critical condition before donation, CT or MRCP could not be performed. To assess the vessels and bile ducts of the liver graft of each recipient, we routinely performed the follow-up CT or MRCP study at 1, 2, and 4 months after LT. In some instances, it was undertaken earlier if unexpected abnormal laboratory data or unexpected clinical conditions (such as unexplainable fever, changed hemodynamics, etc) occurred. PA of the hepatic artery, either intrahepatic or extrahepatic, was defined from tri-phase CT or MRCP or hepatic arteriography. The time lapse between the LT and the diagnosis of the PA, clinical manifestations, clinical data, treatment options, and so forth, were collected.

Factors Affecting Outcomes of Those With Pseudoaneurysm After Liver Transplantation To assess the significant factors affecting the treatment outcome, our sample is small (3 cases). To analyze the factors, not only our patients but also the patients with PA reported in the literature (including 10 case series [Table 2] and 23 case reports [Table 3]) [1e26] were enrolled for analysis. To analyze the significant factors affecting survival, the data were collected from the available description in the literature, including age, sex, clinical manifestation such as bleeding (including gastrointestinal bleeding hemobilia or intra-abdominal bleeding), treatment (with embolization or surgical exploration or stent), diagnosis establishment before (the so-defined “early detection”) or after bleeding, and so forth. In some literature, some patients whose data had not been clearly mentioned were excluded in the analysis about that factor.

Statistical Analysis Comparisons between the groups of survival and of death were made using SPSS (Chicago, Ill, United States). All the data are reported as mean  SD. Comparisons between different groups for each point were performed using 1-way analysis of variance (ANOVA) and multivariate analysis. All tests were 2-tailed, and a value of P < .05 was considered significant.

RESULTS Case Presentation

Among our 50 patients, during the study period, PA of the hepatic artery was found in 3 patients. Diagnosis was established after emergency arteriography in 2 patients after unexpectedly massive bleeding. A silent PA of the third patient was detected incidentally after a regular follow-up CT study. A 43-year-old man received cadaveric donor LT for alcoholic liver cirrhosis (Child-Pugh class C, with esophageal varices (EV) bleeding, refractory ascites, and pleural effusion). The intraoperative and immediate postoperative courses were smooth. However, jaundice developed on the postoperative 3rd week. The abdominal CT scan showed a stenosis of the bile duct anastomosis. Endoscopic retrograde biliary drainage (ERBD) with stent placement (Boston Scientific, 10F, 10 cm) failed, and, subsequently, a percutaneous trans-hepatic biliary drainage (PTBD) (BIOTEQ CORPORATION, Taipei, Taiwan) was established. A sudden onset of massive hemobilia (Hb dropped to

Authors (Year) (Ref. No)

Madariaga (1992) [1]

7

Marshall (2001) [2]

13

Turrion (2002) [3] Kim (2005) [4]

4 11

Fistouris (2006) [5]

12

Jain (2006) [6]

4

Heidenhain (2010) [7]

3

Panaro (2013) [8]

9

Saad (2013) [9]

20

Volpin (2014) [10]

16

Clinical Presentation

Interval After L.T. (Days)

IA bleeding (2) GI bleeding (4) [including rectal bleeding (1)] Liver abscess (1) Pancreatitis (2) Rupture (3) IA bleeding (3) GI bleeding (2) Dropped Hb (2) Fever (1) Pain (1) None, US detected (3) Rupture, hemoperitoneum Hypotension (5) Abnormal LFT (1) Incidental (6) Hypotension (6) GI bleeding (5) Abdominal pain (4) IA bleeding (1) Hemobilia (1) (-)

10e70

Bleeding (1) Livr function impaired (1) Bleeding (4) Fever (3) Asymptomatic (3) Hypotension (12) GI bleeding (7) Dropped hematocrit without symptoms (1) Sepsis (2) Shock (13) Pain (2) GI bleeding (1)

28e1460

Diagnostic Imaging Studies

Treatment

Outcome

Mortality

Arteriography

Ligation

4 Survived

42.80%

8e132

US, DSA (4) DSA (4) Exploration (4) Autopsy (1)

Embolizatin (6) Ligation (3) Excision (1) Revascularization (1) Conservative (1) No treatment (1)

4 Survived (including 2 retransplantation)

69.20%

7e40

Arteriography (10)

No treatment

Died (-)

100% (-)

14e2000

Laparotomy (6) Arteriography (4) Exploration (1) Autopsy (1)

Ligation (6) Excision (3) Embolization (1) None (2)

6 Survived (including 5 retransplantation)

50.0%

(-)

Embolization (1) Resection (1) Observation (1) Ligation (1) Endovascular aortic repair (1)

1 Survived (ligation retransplantation) 1 Survived (retransplantation) 8 Survived

75.0%

1e482

22e92

1 to 1098 median: 90 (iatrogenic) (n¼11) 16 (spontaneous) (n¼9) 4e100

CT CT arteriography CT (7) D-US (2)

Reversed saphenons bypass with anticoagulant (9)

HEPATIC ARTERY PSEUDOANEURYSM AFTER LIVER TRANSPLANT

Table 2. Summary of Series of Patients With Hepatic Artery Pseudoaneurysm After Liver Transplantation in Literature Number of Cases

66.7% 11.1%

Arteriography

TAE 4 (3 failed) Stent graft 8 (1 failed) Surgery (2) Retransplant (6)

7 Died

35.0%

CT (2) US and arteriography (1) Arteriography (11) Post-mortem exam (2)

Treated before rupture (3, all survived) Excision þ Revascularization (7) (28% mortality) Hepatic artery ligation (5) (60% mortality, 1 retransplantation) Endovascular treatment (2) Died without treatment (2)

7 Died

41.2%

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The number in the parenthesis of clinical presentation, diagnosis and treatment represent the patient number. Abbreviations: CT, computed tomographic scan; DSA, digital subtraction; DSA, digital subtraction angiography; D-US, doppler ultrasound; TAE, transcatheter hepatic arterial embolization; IA, intraabdominal; GI, gastrointestinal.

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Table 3. Summary of Case Reports Less Than 3 Cases With Hepatic Artery Pseudoaneurysm After Liver Transplantation in Literature Authors (Years)

Number of Patients

Age

Sex

(-) F F M F

Biliary leak, hemoperitoneum Hematemesis, hypotension Hemobilia, fever Hemobilia, abdominal pain UGI bleeding

Petal (2003) [11] Slater (2004) [12] Finley (2005) [13]

1 1 2

Maleux (2005) [14]

1

(-) 38 55 46 69

Elias (2007) [15]

1

47

M

Adani (2008) [16]

1

60

Jarzembowski (2008) [17] Jiang (2008) [18] Jones (2008) [19]

1

Clinical Presentation

Interval after L.T.

1 month 2 months

Detection Before or After Bleeding

Diagnostic Imaging Studies

Arteriography Arteriography

Arteriography

Pain

16 months

Before

CT

M

GI bleeding

3 months

After

CT

48

F

GI bleeding

1 month

After

Arteriography

(-) 2

(-) 6 15

(-) M F

Biliary leak, hemoperitoneum IA bleeding Rising liver enzyme

1 month 10 days 21 days

After After Before

Arteriography Postmortem exam D-US, CT

Lee CC (2008) [20]

1

54

M

Duodenal bleeding, shock

7 days

After

Arteriography

Kim (2011) [21]

2

16 55

F M

IA bleeding, shock Abdominal discomfort.

14 days 30 days

After After

Arteriography Arteriography

Ou (2011) [22]

1

67

F

5 days

After

CT

Elsharkawy (2012) [23] Lu (2012) [24]

1 2

Harda (2013) [25]

1

59 53 55 40

M F M M

Massive subcapsular bleeding with right pleural effusion Graft dysfunction Routine follow-up Pain, bile leak Hematemesis, jaundice

3 months 6 months 30 days 8 years

After Before Before After

Arteriography Colon doppler US U1., CT

Mossdorf (2013) [26]

1

(-)

(-)

Rising inflammation parameters

6 weeks

Before

CT

Treatment

Outcome

Embolization Balloon and stent Resection with graft Resection with graft Embolization rebleeding 3rd week stent graft Balloon angioplasty and a Jomed stent graft to exclude PA Exploration, aorto-hepatic hypass, failed, retransplantation Reoperation revascularization using an artery conduct Embolization No treatment Embolization and ligation of hepatic artery Embolization, retransplantation 30th months Excision and artery interposition stent graft Balloon-expaendable stent Embolization

Survived Survived Survived Survived Survived

Mutilayered stent Balloon-expandable covered stent graft Embolization, rebleeding 25th date, retransplantation Stent graft

Survived Survived Survived Survived

Abbreviations: CT, computed tomographic scan; D-US, doppler ultrasound; UGI, upper gastrointestinal tract; GI, gatrointestinal tract; IA, intraabdominal; H.A., hepatic artery; US, ultrasound.

Survived

Died

Survived

Died Survived Survived Died (H.A. thrombosis) Survived Survived

Survived

JENG, HUANG, LIN ET AL

2 months

After After After After After

HEPATIC ARTERY PSEUDOANEURYSM AFTER LIVER TRANSPLANT

3.9 g/dL) with hypovolemic shock occurred the next day. After resuscitation, emergency arteriography was undertaken and showed a ruptured PA at the right hepatic artery (Fig 1). Transcatheter hepatic arterial embolization with micro-coils was attempted but failed. Emergency laparotomy to repair of the bleeder was undertaken. The patient died of prolonged shock and multi-organ failure. Another 62-year-old man received living related donor liver transplantation (LRDLT) with right liver graft from his daughter for hepatitis B viral infection (HBV)-related liver cirrhosis (Child-Pugh class B), with a hepatocellular carcinoma (HCC) at hepatic segments 6 and 7 (cT2N0M0, stage II). Before transplantation, he had received repeated sessions of endoscopic ligation for EV bleeding and transcatheler hepatic arterial chemo-embolization (TACE) for HCC. The operation and postoperative courses were smooth. Five months after the operation, a sudden onset of epigastragia and massive hematochezia occurred (Hb dropped to 7.4 g/dL). Endoscopy showed massive bleeding at the duodenal area. After arteriography (Fig 2), emergency exploration found a ruptured PA of the hepatic artery near the bile duct with massive bleeding into the duodenum. Repair of the artery for hemostasis was done, but the patient died of multi-organ failure 5 days later. The third case was a 54-year-old man with HBV-related liver cirrhosis and HCC in bilateral lobes. After 2 sessions of TACE to downstage the HCC to meet the transplantation criteria, he received LRDLT with right liver graft from his son. The postoperative course was smooth. He received pulse therapy for acute cellular rejection after pathological confirmation by liver biopsy 3 months after the operation. For the occurrence of biliary stricture, after the failure of ERBD, he received PTBD with 3 subsequent

Fig 1. Rupture of a pseudoaneurysm (white arrow) of proper hepatic artery with severe vasoconstriction and reflux of contrast medium into abdominal aorta.

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Fig 2. Rupture of a pseudoaneurysm of right hepatic artery (white arrow) with extravasation of contrast medium outlining the blood clot in common bile duct (CBD) and severe vasoconstriction. There is a plastic endoscopic retrograde bile duct (ERBD) stent from the hilar bile duct to the duodenum for the stenosis at the biliary anastomostic site.

consecutive sessions of PTBD revision. The regular follow-up CT scan on the 4th month after LT showed a PA of the intrahepatic hepatic artery (Fig 3). The PA remains silent without symptoms and signs of bleeding. However, to avoid the potential rupture, we undertook hepatic

Fig 3. A vascular stent was placed at the anastomostic stenosis to exclude the pseudoaneurysm (white arrow) of posterior segmental hepatic artery.

1154

arteriography with a transluminal angioplasty with placing a stent for the stenotic artery to exclude of the PA smoothly. The patient was well up to 16 months without any symptoms. Two patients whose PA was detected after rupture died. The third patient whose PA was detected prior to rupture was successfully treated and survived. Analysis of Factors Affecting Survival

Among the case series (Table 2), mortality rate ranged variably, from 11.1% to 100% (median, 50%). From univariate analysis, the significant factors affecting survival were female (sex) (P ¼ .036), stent treatment (P ¼ .006), and early detection (P ¼ .036), whereas age (P ¼ .493) and presentation as hemorrhage (P ¼ .877) were not significant factors. From multivariate analysis, stent treatment has a borderline significance (P ¼ .056). DISCUSSION

PA of the hepatic artery after LT is rare, with an incidence of about 2%, but is potentially catastrophic [2,3,5,6,16,19,20]. The most common presentation of PA of the hepatic artery is rupture with massive hemorrhage [1e26]. It may rupture into the adjacent liver, portal, or biliary system, or directly into the abdominal cavity. The manifestations include intra-abdominal bleeding, gastrointestinal hemorrhage, hemobilia, sometimes accompanied by jaundice or fever, hypotension, or death [1e26]. PA can be classified as intrahepatic or extrahepatic, according to the location [3,4,9,13]. The majority of extrahepatic PAs are “spontaneous,” usually at the hepatic arterial anastomosis. The most important contributing factor is local sepsis probably related to immunosuppression, biloma, biliary tract infection, and so forth [1e16,19]. Intrahepatic PAs are rare in comparison to extrahepatic ones and may present as subclinical or incidental findings on radiological images. The causes of intrahepatic PAs are usually iatrogenic (percutaneous trans-hepatic procedures, such as percutaneous trans-hepatic cholangiography, biopsies, endoscopically placed biliary stents, and hepatic artery balloon angioplasty [9,22,25]), whereas it still has a potential of severe hemorrhage. The PA of our case 1 and case 2 is extrahepatic and that of case 3 is intrahepatic. All of them received many sessions of percutaneous or biliary interventions such as ERBD, PTBD, and liver biopsy. The factors of local infection, introgenic cause, and immunosuppression are present in all 3 cases. Sometimes it is difficult to define clearly the main cause of the development of PA. In our study, the overall mortality rate of these 3 patients is as high as 66.7%. Both the two patients with unexpectedly sudden massive bleeding died despite emergency exploration. We attribute the survival of our third patient to the early detection before the rupture. From our analysis, including our cases and the cases in literature, early detection (detection of PA prior to the rupture of PA) and stent treatment are two significant determinants of survival.

JENG, HUANG, LIN ET AL

Early detection contributes to a better survival rate because the treatment of ruptured PAs is usually difficult. Socalled “early detection” means that the PA is detected prior to the rupture presentation and does not mean the time interval (the postoperative “early” days). The detection day of our third patient (who survived) is 123 days, but those of the first 2 patients (who died) are 23 days and 153 days, respectively. Song et al [27], in a report presented in 2015, had 2 cases of PA of the hepatic artery [27]. Both were discovered incidentally during routine follow-up CT. For both, the detection is early because it is prior to rupture. The detection days after the LT were 2274 days and 1605 days, respectively. One kept observation and the other received excision with hepatic artery revision [27]. From the literature, PA may develop late. The days may be as late as more than 1000 days [27]. The regular follow-up CT or MRI must be continued to detect “early” before the occurrence of rupture. In the absence of rupture or infection, successful treatment with primary repair by resection and re-anastomosis, or by reconstruction with an artery graft or stent or by angioplasty or embolization, had been reported individually in literature [8,11e15,17,19e26]. However, direct reconstruction is not feasible in the field of infection or of massive hemorrhage. On that occasion, the damaged artery is usually beyond repair. Unfortunately, in most cases, when active bleeding occurs, to sacrifice the hepatic artery may be unavoidable, which usually equates with graft necrosis or loss, and a retransplantation of liver is needed but becomes critical. Stent treatment is another key determinate of survival. It may preserve the hepatic artery and avoids ligation or embolization, whereas the feasibility of stent placement depends on early detection and the PA location. Early detection of such a life-threatening complication is a key determinant of survival; this means the detection of the PA incidentally prior to the rupture manifestation. To early detect the PA and to undertake the postoperative follow-up imaging studies such as CT scan or MRCP early and periodically is strongly recommended, especially for those who had received other percutaneous or biliary interventions before or after liver transplantation. REFERENCES [1] Madariaga J, Tzakis A, Zajko AB, et al. Hepatic artery pseudoaneurysm ligation after orthotopic liver transplantation: a report of 7 cases. Transplantation 1992;54:824e8. [2] Marshall MM, Muiesan P, Srinivasan P, et al. Hepatic artery pseudoaneurysms following liver transplantation: incidence, presenting features and management. Clin Radiol 2001;56:579e87. [3] Turrión VS, Alvira LG, Jimenez M, et al. Incidence and results of arterial complications in liver transplantation: experience in a series of 400 transplants. Transplant Proc 2002;34:292e3. [4] Kim HJ, Kim KW, Kim AY, et al. Hepatic artery pseudoaneurysms in adult living-donor liver transplantation: efficacy of CT and Doppler sonography. Am J Roentgenol 2005;184:1549e55. [5] Fistouris J, Herlenius G, Bäckman L, et al. Pseudoaneurysm of the hepatic artery following liver transplantation. Transplant Proc 2006;38:2679e82. [6] Jain A, Costa G, Marsh W, et al. Thrombotic and nonthrombotic hepatic artery complications in adults and children

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[18] Jiang XZ, Yan LN, Li B, et al. Arterial complications after living-related liver transplantation: single-center experience from West China. Transplant Proc 2008;40:1525e8. [19] Jones VS, Chennapragada MS, Lord DJE, et al. Post-liver transplant mycotic aneurysm of the hepatic artery. J Pediatr Surg 2008;43:555e8. [20] Lee CC, Jeng LB, Poon KS, et al. Fatal duodenal hemorrhage complicated after living donor liver transplantation: case report. Transplant Proc 2008;40:2840e1. [21] Kim SJ, Yoon YC, Park JH, et al. Hepatic artery reconstruction and successful management of its complications in living donor liver transplantation using a right lobe. Clin Transplant 2011;25:929e38. [22] Ou HY, Concejero AM, Yu CY, et al. Hepatic arterial embolization for massive bleeding from an intrahepatic artery pseudoaneurysm using N-butyl-2-cyanoacrylate after living donor liver transplantation. Transpl Int 2011;24:19e22. [23] Elsharkawy AM, Sen G, Jackson R, et al. Use of a multilayered stent for the treatment of hepatic artery pseudoaneurysm after liver transplantation. Cardiovasc Intervent Radiol 2012;35: 207e10. [24] Lu NN, Huang Q, Wang JF, et al. Treatment of post-liver transplant hepatic artery pseudoaneurysm with balloon angioplasty after failed stent graft placement. Clin Res Hepatol Gastroenterol 2012;36:109e13. [25] Harada N, Shirabe K, Soejima Y, et al. Intrahepatic artery pseudoaneurysm associated with a metallic biliary stent after living donor liver transplantation: report of a case. Surg Today 2013;43: 678e81. [26] Mossdorf A, Ulmer T, Kalverkamp S, et al. Transposition of the hepatic artery as a salvage procedure for an aortic pseudoaneurysm after liver transplantation. Liver Transpl 2013;19: 105e7. [27] Song S, Kwon CH, Moon HH, et al. Single-center experience of consecutive 522 cases of hepatic artery anastomosis in living-donor liver transplantation. Transplant Proc 2015;47: 1905e11.