© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Clin Transplant 2014: 28: 1305–1312 DOI: 10.1111/ctr.12431
Clinical Transplantation
Review Article
Surgical and endovascular treatment of hepatic arterial complications following liver transplant Chen J, Weinstein J, Black S, Spain J, Brady PS, Dowell JD. Surgical and endovascular treatment of hepatic arterial complications following liver transplant. Abstract: Vascular complications after liver transplantation increase post-operative morbidity and contribute to the incidence of retransplantation. Vascular complications comprise arterial, caval, and portal venous pathology, with the majority of complications being arterial in etiology, including anastomotic stricture, pseudoaneurysm, and thrombosis. There are two major therapeutic options for the treatment of these arterial complications: endovascular intervention and surgery. The former includes intra-arterial thrombolysis, embolization, percutaneous transluminal angioplasty, and stent placement. The latter includes thrombectomy, reanastomosis, and retransplantation. Although surgical treatment has been considered the first choice for management in the past, advances in endovascular intervention have increased and make it a viable therapeutic option following orthotopic liver transplantation. This review focuses on the role of surgical and endovascular therapy in the management of hepatic arterial complications after liver transplantation.
Jun Chena,*, Jeffrey Weinsteinb, Sylvester Blackc, James Spaina, Paul S. Bradyb and Joshua D. Dowella a
Division of Interventional Radiology, Department of Radiology, Wexner Medical Center, The Ohio State University, Columbus, OH, bDivision of Interventional Radiology, Department of Radiology, Einstein Medical Center, Philadelphia, PA and cThe Division of Transplant Surgery, Department of Surgery, Wexner Medical Center, The Ohio State University, Columbus, OH, USA Key words: arterial vascular complication – endovascular therapy – liver transplant – stenting Corresponding author: Joshua D. Dowell, MD, PhD, 395 W 12th Ave., Suite 424, Columbus, OH 43210, USA. Tel.: 614-685-6793; fax: 614-293-69365; e-mail: [email protected] *Jun Chen was a visiting scholar at The Ohio State University during 2013. He was sponsored by Jiangsu Government Scholarship for Overseas studies, China. He is currently working at the Division of Interventional Radiology, Department of Radiology, Jiangsu Cancer Hospital & Cancer Hospital of Nanjing Medical University (NMU), Nanjing, China. Conflict of interest: None. Accepted for publication 31 July 2014
Liver transplantation is a life-saving treatment for patients with end-stage liver disease, acute liver failure (ALF), hepatocellular carcinoma, and other diseases (1–4). Vascular complications after
liver transplantation increase post-operative morbidity and contribute to the incidence of retransplantation (5). The overall incidence of vascular complications after liver transplantation is
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7.2–30.8% (5–9). These vascular complications can be divided into predominantly three classes: arterial (4.8–16.6%), portal (1.2–12.3%), and caval etiologies (1.2%) (5, 8, 9). The associated morbidity of hepatic arterial complications (HAC) is significant, and surgical reconstruction of the hepatic artery for post-operative arterial thrombosis is often graft saving and life saving (10, 11). More recently, advances in endovascular therapy have led to an increasing role of transcatheter approaches for HAC following liver transplantation, including hepatic artery anastomotic stenosis (HAS), hepatic artery pseudoaneurysm (HAP), and hepatic artery thrombosis (HAT) (11–14). This review focuses on the recent applications of surgical and endovascular therapies in the management of hepatic arterial complications after liver transplantation. Etiology of hepatic arterial complications following liver transplantation
The etiology underlying most HAC involves the anastomosis, including (i) hepatic artery anastomotic stricture (0.8–9.3%), (ii) pseudoaneurysm formation (0–3%), and (iii) thrombosis (1.9– 16.6%) (5, 6, 9, 15–17). Hepatic artery stenosis
Hepatic artery anastomotic stenosis, oftentimes subclinical in presentation, may contribute to an insidious form of graft dysfunction. Stenosis may progress to hepatic artery thrombosis, lead to biliary complications as well as eventual graft loss both in the early and late post-operative periods (18). Etiologies of HAS may include allograft rejection, microvascular injury associated with the cold preservation of the liver, or a disrupted vasa vasorum (18–20). Vascular clamp injuries, differences between donor and recipient vessel calibers as well as extrinsic compression, may also lead to HAS (18–20). However, the use of surgical loupes at time of transplantation has been shown to reduce operative time and provide superior patency compared with performing the arterial anastomosis under a surgical microscope (21). Low intra-operative hepatic artery and portal vein flow at the time of transplant also correlates with an increased risk for anastomotic stenosis (22). Interestingly, patients with a presumed underlying immunologic basis for their orthotopic liver transplantation (OLT), such as autoimmune hepatitis, primary biliary cirrhosis, or primary sclerosing cholangitis, do not show a significantly increased risk for postOLT HAS (18).
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Hepatic artery pseudoaneurysm
Hepatic artery pseudoaneurysms most commonly result from surgical manipulation of the hepatic artery or surrounding structures. Additionally, HAPs have been described secondary to salvage procedures related to thrombolysis and angioplasty for hepatic artery stenosis (23, 24). Risk factors for the development of intrahepatic HAPs are interventional procedures such as liver biopsy, percutaneous transhepatic cholangiography, and the placement of transhepatic drainage catheters, while the most important risk factor for extrahepatic HAP is local sepsis (25). Although HAPs may remain asymptomatic and are usually found serendipitously on ultrasound examinations performed post-transplantation, they have potentially severe consequences, such as rupture with consequent hemobilia and intraperitoneal hemorrhage (23, 24, 26). Hepatic artery thrombosis
Hepatic artery thrombosis is categorized by the timing of the event post-transplantation, either as early in the post-operative phase or late. Early HAT refers to thrombosis occurring within two months after liver transplantation (27), whereas late HAT occurs beyond this two-month window. HAT is associated with acute rejection, positive cytomegalovirus serology in the donor, polytransfusion, the use of aortic conduits, variant arterial anatomy, as well as unmatched vessel caliber between the donor and recipient (27–29). Additionally, cold ischemia and prolonged operative times have been linked to HAT following liver transplantation (27–29). Roux-en-Y biliary reconstruction, graft revision, and reoperation are also identified risk factors (28). Graft ischemia in liver transplant recipients caused by HAS and/or HAT contributes significantly to mortality and graft loss after liver transplantation (18, 27, 30, 31). Treatment approaches
There are currently two major therapeutic options for the treatment of these arterial complications: endovascular interventions and surgery (11, 31, 32). The former includes intra-arterial thrombolysis, embolization, percutaneous transluminal angioplasty (PTA), and stent placement. The latter includes thrombectomy, anastomotic reconstruction, and retransplantation. While surgical intervention is often considered the first choice for the management of early HACs, advances in endovascular interventions may make these modalities an acceptable alternative option in many instances.
Arterial complications after liver transplant Hepatic artery anastomotic stricture
Surgical options for the treatment of HAS include resection of the stenotic segment with reanastomosis, aortic conduit graft, interposition vein graft, vein patch angioplasty, or interposition artery graft (18). Revision of the hepatic artery (HA) may help prevent biliary strictures and allow for good long-term graft function in the majority of patients (18). In a previous study, post-revisional HA patency was demonstrated in 78% of cases with revised hepatic arterial anastomoses, and the actuarial patient and graft survivals at four yr were 65% and 56%, respectively (18). Table 1 shows the outcomes of HAS treated by endovascular interventions and surgery in previous studies. The literature supports that endovascular treatment can be successfully performed for HAS and decreases the need for surgical revascularization and liver retransplantation (Fig. 1). The reported PTA and stent placement were safely performed three d to 68 months after liver transplant (Table 1). A study using ultrasound to evaluate the patency of HA demonstrated that both PTA and stent placement can improve HA peak systolic velocity and resistive indices on ultrasound images in HAS patients (33). The primary patency rates after primary stent placement were reported as 92%, 85%, and 69% at one, three, and six months, respectively, compared with 70%, 60%, and 50% after PTA (34). Initial use of a stent may improve primary patency whencomparedwithPTA (35,36). Hepatic artery anastomotic stenosis recurrence is sometimes encountered in patients after transluminal interventional therapy for thrombosis and HAS. Repeated endovascular treatments for recurring HASs have been shown feasible with a high
technical success rate (94.6% hepatic artery patency) and contributed to favorable long-term results (87.7% patient survival in five yr) (19). Nevertheless, endovascular treatment may be unsuccessful in some HAS patients, and to date, this patient population cannot be predicted. Surgical therapy is indicated in such situations. PerezSaborido et al. reported four HAS cases of whom three patients were unsuccessfully treated by percutaneous angioplasty with stent placement. Surgical treatments were then effectively performed in these three patients (5). Hepatic artery pseudoaneurysm
Arteriography should be performed in suspected cases of HAP and is the examination of choice to plan further treatment (25). Coil embolization can be used emergently to achieve hemostasis in unstable patients presenting with pseudoaneurysm rupture, but the resultant hepatic artery occlusion may lead to subsequent graft ischemia (37, 38). Superselective embolization techniques in patients with intrahepatic HAP allow preservation of arterial supply to the graft, with no adverse effect on graft function (25). The small caliber of hepatic arteries initially made stent placement challenging due to the lack of available commercially produced stents; however, the remodeling ability of modern balloon-expandable covered stent grafts has recently been shown to allow adequate exclusion of the pseudoaneurysm and preserve flow in patients with HAP (39) (Fig. 2). Table 2 shows the outcomes of HAP treated by endovascular interventions and surgery in previous studies (40–42). Both hepatic artery ligation and embolization, used as a temporary measure for control of acute
Table 1. Hepatic artery stenosis treated by endovascular interventions and surgery in previous studies
Author (year)
n
Timing from transplant
Frongillo (2013) (15) Hamby (2013) (33) rez-Saborido (2011) (5) Pe kova (2010) (34) La stovic Maruzzelli (2010) (35) da Silva (2008) (20) Huang (2006) (36) Abbasoglu (1997) (18)
10 23 3 19 24 8 14 41
10 m/1–24 m 92.5 d/12–236 d Not reported 2.7 m/3 d–6 m 15.8 m/5–58 m 14.2 m/9–68 m 3-225 d 100/1–1220 d
Management (n) PTA + Stent (10) PTA (10), Stent (13) Surgical treatment (3) PTA + Stent (15), PTA (4) PTA (13), Stent (11) Stent (6), PTA (2) Stent (14) Reanastomosis (17), aortohepatic iliac artery graft (11), interposition vein graft (4), vein patch angioplasty (2), interposition artery graft (1), PTA (6)
Immediate technical success 100% 97.1% 100% 100% 96% 88.9% 85.7% 78% in total, 100% in PTA
Required reintervention, retransplantation or revascularization Not reported 43.5% 0% 15.8% 29.2% 50% 7.1% 17.9%
d, days; m, months; PTA, percutaneous transluminal angioplasty.
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A
B
A
D
Fig. 1. Hepatic artery anastomotic stricture following liver transplantation. (A) Digital subtraction angiography revealing high-grade hepatic arterial anastomotic stricture (arrow) in a 61-yr-old patient post-liver transplantation and (B) its resolution following stent placement across the stenosis (arrow).
B
E
C
F
hemorrhage, can facilitate subsequent successful retransplantation (23, 25). Given surgical revascularization or retransplantation for HAP may be associated with a high mortality rate of up to 69% (25), surgical management is reserved for more complicated cases and indicated when endovascular techniques fail (37, 38). Hepatic arterial thrombosis
Early HAT may lead to graft ischemia and biliary necrosis and is associated with significant graft loss and mortality (27). It was reported that graft survivals were 79% vs. 71% and 50% vs. 50% at one and three yr, respectively, for early HAT and late HAT (43). Because arterial collateralization takes between three wk and four months following arterial thrombosis, graft salvage depends on early detection, limiting warm ischemia and urgent revascularization (8). Therefore, early identification and treatment is critical to recover blood flow
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Fig. 2. Hepatic artery pseudoaneurysm following liver transplantation. (A) Color Doppler ultrasound revealing a large pseudoaneurysm with high turbulent flow in a 50-yr-old patient post-liver transplantation. Select axial (B) and coronal (C) images from CT angiogram confirming a large hepatic arterial anastomotic pseudoaneurysm (arrows). Digital subtraction angiography (D) further delineates the anastomotic pseudoaneurysm (arrow) without involvement of the right or left hepatic artery and (E) its exclusion following covered stent placement across the pseudoaneurysm (arrow). (F) Coronal MIP on follow-up CT angiogram demonstrating stent patency and exclusion of the pseudoaneurysm (arrow).
to rescue the graft. Doppler ultrasonography examination performed at 24 and 48 hr after transplantation can be used as a screening protocol for the early diagnosis of HAT (31). Magnetic resonance angiography (MRA) complements Doppler ultrasound to exclude significant hepatic artery stenosis (44). Computer tomography angiography (CTA) is highly accurate in identifying hepatic artery thrombosis after liver transplantation (45). Treatment of HAT usually requires a surgical intervention including immediate liver retransplantation; however, this option is limited by organ availability (28). Table 3 shows the outcomes of HAT treated by endovascular interventions and surgery in previous studies. Vrochides et al. reported that mean graft survival of 24 HAT patients treated by surgical thrombectomy and arterial reanastomosis was 48.8 months and mean patient survival was 101.2 months (46). Urgent revascularization in cases of early HAT may decrease graft loss, especially when within
Arterial complications after liver transplant Table 2. Hepatic artery pseudoaneurysm treated by endovascular interventions and surgery
Author (year)
n
Timing from transplant
Saad (2013) (37) Chen (2012) (40) Lu (2012) (39) Ou (2010) (41) Ginat (2009) (24) Jones (2008) (16)
12 1 1 1 1 1
157 d/1–1098 d 1d 6m 45 d Not reported 2 wk
Fistouris (2006) (23)
9
39.5 d/14 d–5 yr
Banga (2005) (42) Marshall (2001) (39)
2 11
Lowell (1999) (26)
7 wk, 15 m 30 d/8–132 d
2
Not reported(1), 4 m (1)
Management (n) Embolization (4), Stent (8) Embolization (1) Stent (1) Embolization (1) Stent (1) Embolization followed by surgical excision (1) Surgical excision (3), retransplantation (4), ligation (2) Stent (2) Embolization (6), ligation (3), excision (1), revascularization (1) Surgical reconstruction followed by PTA (1), Surgical repair (1)
Immediate technical success (%)
Normal hepatic flow by ultrasound (%, follow-up time)
83.3% 100% 100% 100% 100% 100%
70% (4.9 m/0-18 m) Not reported 100% (5 m) 100% (6 m) 100% (6 m) 100% (6 wk)
100%
100% in 5 patients from 1996 to 2005 (4.2 yr/7.4 m–6.9 yr)
100% 100%
100% (15 d, 3 yr) Not reported
100%
100% (24 m, 21 m)
d, days; wk, week; m, months; yr, years; PTA, percutaneous transluminal angioplasty.
Table 3. Hepatic artery thrombosis treated by endovascular interventions and surgery
Author (year)
n
Timing from transplant
Intervention (n)
Outcome (follow-up time)
Mali (2012) (8) Grodzicki (2011) (31)
4 23
0 d–1 m Not reported
Retransplant (3), Thrombectomy (1) Retransplant (17), Endovascular (6)
rez-Saborido (2011) (5) Pe Wu (2011) (17)
7 14
Not reported 10/1–41 d
Singhal (2010) (48) Vrochides (2010) (46)
1 24
1d Not reported
Kim (2006) (49) Pinna (1996) (50)
2 17
6 and 4 hr 11 d
Retransplant (6), Surgical aortic graft (1) Rearterialization (3), rearterialization and IA thrombolysis (3), IA thrombolysis (2), Retransplant (6) IA thrombolysis (1) Thrombectomy and arterial reanastomosis at the same site (n = 10), at a different site (n = 14) IA thrombolysis (2) Revascularization (10), Revascularization followed by IA thrombolysis (7)
100% alive (not reported) 64.7% alive (not reported), 50% alive, 50% Retransplant (not reported) 85.7% alive (not reported) 58.3% alive (18-66 m), 50% alive (18-66 m)
100% alive (17.5 m) Mean graft survival was 48.8 m
100% alive (7 m, 8 m) 64.7% alive (17 m)
h, hours; d, days; m, month; IA, intra-arterial.
the first week after liver transplant (43). A previous study revealed that graft salvage may achieve 81% when the revascularization was performed within the first week after liver transplant while late revascularization was unsuccessful in all cases (43). Although survival of HAT patients remains high, this recent study verified the necessity of retransplantation whenever the diagnosis of HAT is confirmed, as surgical thrombectomy and anastomotic revision failed to improve graft survival in eight of 24 patients (46). UNOS/ OPTN policy 3.6 (October 13, 2013) allows for the urgent relisting of liver transplant candidates with HAT within seven d of transplantation as
status 1 with evidence of severe liver injury defined as AST ≥ 3000 and one or both of the following INR ≥ 2.5, acidosis defined as arterial pH ≤ 7.30 or venous pH of 7.25 and/or Lactate ≥ 4 mmol/L. For liver transplant, recipients within 14 d of transplantation with a diagnosis of HAT and not meeting the above criteria are listed with a MELD of 40. This policy reflects the understanding that early and acute onset of HAT post-liver transplantation represents a significant cause of mortality and graft loss while late onset HAT may not necessarily need retransplantation secondary to the development of collaterals (47).
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Although surgical revascularization has traditionally been first-line treatment for early HAT, endovascular interventions are rapidly evolving and have recently achieved high success rates (13, 30, 35). If suspicion exists for an arterial complication by ultrasound, the diagnosis should be confirmed by arteriography and, if possible, treatment should be attempted by fibrinolysis, angioplasty, or even stent placement for graft salvage (5). Local thrombolysis can also be used to treat acute HAT occurring immediately after stent deployment (Fig. 3) (35). HAS is a contributor to HAT; however, percutaneous transluminal angioplasty of focal HAS can reduce the incidence of HAT more than threefold (30). Conclusions and future directions
With the evolution of endovascular techniques and improved angioplasty and stent technology, many complications of liver transplant that were traditionally treated surgically may be addressed by an endovascular approach. Endovascular treatment is less invasive than surgical intervention and harbors good overall results; however, surgery should be available in the event endovascular techniques are unsuccessful or not feasible. With respect to HAS, further study is needed into what, if any, features of the patient or lesion will help predict those patients that would benefit
A
B
C
D
E
F
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most from endovascular therapy. Determining these factors is crucial to managing these patients and triaging them to angioplasty or stenting or going directly to surgical revision. There is evidence that primarily stenting these lesions may yield a longer primary patency vs. angioplasty alone. Comparing covered vs. uncovered stents, the potential effectiveness of drug eluting stents or angioplasty with drug eluting balloons are possible areas for future study. Covered stenting is often preferable to surgery in patients with HAP due to a significant mortality rate associated with surgical intervention. Angiography is also important for confirmation of the diagnosis and rapid control of the hepatic artery in cases of pseudoaneurysm rupture. For patients with HAT, Doppler ultrasound shows good sensitivity and specificity in early detection of arterial thrombosis. Arteriography can confirm the diagnosis and select patients for intervention. Of course, rapid restoration of blood flow is a priority in these patients by surgical or endovascular means. Catheter-directed thrombolysis with possible angioplasty and/or stenting has been successfully employed to treat HAT and is an area for future exploration. Continued research to identify the patient factors and lesion characteristics of those patients that would benefit from endovascular revascularization vs. surgery may change the paradigm for treatment of this serious post-transplant complication.
Fig. 3. Hepatic artery stenosis and thrombosis following liver transplantation. (A) Digital subtraction angiography revealing high-grade focal hepatic arterial anastomotic stricture (arrow) in a 57-yr-old patient post-liver transplantation and (B) improved flow following angioplasty at the stenosis (arrow). (C) Subsequent arterial thrombosis apparent on postangioplasty angiography (arrow). (D) Minimal improvement in thrombosis after intra-arterial administration of tPA (arrow). Axial (E) and (F) coronal CT images showing subsequent biloma formation (arrow) after hepatic artery thrombosis, ultimately requiring retransplant.
Arterial complications after liver transplant Vascular complications following liver transplant remain a significant source of morbidity and cause of graft loss requiring retransplantation. Hepatic arterial complications are the most commonly encountered of these vascular complications. Expedient management is imperative for graft salvage. The development of endovascular interventions for managing these complications has added to the armamentarium with good overall success. Improving our understanding of the patient characteristics or surgical techniques that place patients at risk for these complications may avoid or reduce these complications and, in turn, improve patient survival. References 1. MURRAY KF, CARITHERS RL Jr; AASLD. AASLD practice guidelines: evaluation of the patient for liver transplantation. Hepatology 2005: 41: 1407. 2. SCHUPPAN D, AFDHAL NH. Liver cirrhosis. Lancet 2008: 371: 838. 3. MOON DB, LEE SG. Liver transplantation. Gut Liver 2009: 3: 145. 4. DECAENS T. Liver transplantation for hepatocellular carcinoma: time for an international consensus. Clin Res Hepatol Gastroenterol 2012: 36: 316. -SABORIDO B, PACHECO-SANCHEZ D, BARRERA-REBOL5. PEREZ LO A et al. Incidence, management, and results of vascular complications after liver transplantation. Transplant Proc 2011: 43: 749. € K, ENNE M, FERNANDES R et al. Vascular 6. STEINBRUCK complications after living donor liver transplantation: a Brazilian, single-center experience. Transplant Proc 2011: 43: 196. 7. SINTRA SN, TOME L, CIPRIANO MA, BENTO C, FURTADO E. Long-term outcome of the first 150 liver transplant recipients: a single-center experience. Transplant Proc 2013: 45: 1119. 8. MALI VP, AW M, QUAK SH, LOH DL, PRABHAKARAN K. Vascular complications in pediatric liver transplantation; single-center experience from Singapore. Transplant Proc 2012: 44: 1373. 9. MESQUITA MC, FERREIRA AR, VELOSO LF et al. Pediatric liver transplantation: 10 years of experience at a single center in Brazil. J Pediatr (Rio J) 2008: 84: 395. 10. HEFFRON TG, PILLEN T, WELCH D, SMALLWOOD GA, REDD D, ROMERO R. Hepatic artery thrombosis in pediatric liver transplantation. Transplant Proc 2003: 35: 1447. 11. WAKIYA T, SANADA Y, MIZUTA K et al. A comparison of open surgery and endovascular intervention for hepatic artery complications after pediatric liver transplantation. Transplant Proc 2013: 45: 323. 12. BOYVAT F, AYTEKIN C, KARAKAYALI H, HABERAL M. Interventional radiology in liver transplant. Exp Clin Transplant 2008: 6: 105. 13. KARANI JB, YU DF, KANE PA. Interventional radiology in liver transplantation. Cardiovasc Intervent Radiol 2005: 28: 271. 14. AZZAM AZ, TANAKA K. Management of vascular complications after living donor liver transplantation. Hepatogastroenterology 2012: 59: 182. 15. FRONGILLO F, GROSSI U, LIROSI MC et al. Incidence, management, and results of hepatic artery stenosis after liver
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Clin Transplant 2014: 28: 1305–1312 DOI: 10.1111/ctr.12431
Clinical Transplantation
Review Article
Surgical and endovascular treatment of hepatic arterial complications following liver transplant Chen J, Weinstein J, Black S, Spain J, Brady PS, Dowell JD. Surgical and endovascular treatment of hepatic arterial complications following liver transplant. Abstract: Vascular complications after liver transplantation increase post-operative morbidity and contribute to the incidence of retransplantation. Vascular complications comprise arterial, caval, and portal venous pathology, with the majority of complications being arterial in etiology, including anastomotic stricture, pseudoaneurysm, and thrombosis. There are two major therapeutic options for the treatment of these arterial complications: endovascular intervention and surgery. The former includes intra-arterial thrombolysis, embolization, percutaneous transluminal angioplasty, and stent placement. The latter includes thrombectomy, reanastomosis, and retransplantation. Although surgical treatment has been considered the first choice for management in the past, advances in endovascular intervention have increased and make it a viable therapeutic option following orthotopic liver transplantation. This review focuses on the role of surgical and endovascular therapy in the management of hepatic arterial complications after liver transplantation.
Jun Chena,*, Jeffrey Weinsteinb, Sylvester Blackc, James Spaina, Paul S. Bradyb and Joshua D. Dowella a
Division of Interventional Radiology, Department of Radiology, Wexner Medical Center, The Ohio State University, Columbus, OH, bDivision of Interventional Radiology, Department of Radiology, Einstein Medical Center, Philadelphia, PA and cThe Division of Transplant Surgery, Department of Surgery, Wexner Medical Center, The Ohio State University, Columbus, OH, USA Key words: arterial vascular complication – endovascular therapy – liver transplant – stenting Corresponding author: Joshua D. Dowell, MD, PhD, 395 W 12th Ave., Suite 424, Columbus, OH 43210, USA. Tel.: 614-685-6793; fax: 614-293-69365; e-mail: [email protected] *Jun Chen was a visiting scholar at The Ohio State University during 2013. He was sponsored by Jiangsu Government Scholarship for Overseas studies, China. He is currently working at the Division of Interventional Radiology, Department of Radiology, Jiangsu Cancer Hospital & Cancer Hospital of Nanjing Medical University (NMU), Nanjing, China. Conflict of interest: None. Accepted for publication 31 July 2014
Liver transplantation is a life-saving treatment for patients with end-stage liver disease, acute liver failure (ALF), hepatocellular carcinoma, and other diseases (1–4). Vascular complications after
liver transplantation increase post-operative morbidity and contribute to the incidence of retransplantation (5). The overall incidence of vascular complications after liver transplantation is
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7.2–30.8% (5–9). These vascular complications can be divided into predominantly three classes: arterial (4.8–16.6%), portal (1.2–12.3%), and caval etiologies (1.2%) (5, 8, 9). The associated morbidity of hepatic arterial complications (HAC) is significant, and surgical reconstruction of the hepatic artery for post-operative arterial thrombosis is often graft saving and life saving (10, 11). More recently, advances in endovascular therapy have led to an increasing role of transcatheter approaches for HAC following liver transplantation, including hepatic artery anastomotic stenosis (HAS), hepatic artery pseudoaneurysm (HAP), and hepatic artery thrombosis (HAT) (11–14). This review focuses on the recent applications of surgical and endovascular therapies in the management of hepatic arterial complications after liver transplantation. Etiology of hepatic arterial complications following liver transplantation
The etiology underlying most HAC involves the anastomosis, including (i) hepatic artery anastomotic stricture (0.8–9.3%), (ii) pseudoaneurysm formation (0–3%), and (iii) thrombosis (1.9– 16.6%) (5, 6, 9, 15–17). Hepatic artery stenosis
Hepatic artery anastomotic stenosis, oftentimes subclinical in presentation, may contribute to an insidious form of graft dysfunction. Stenosis may progress to hepatic artery thrombosis, lead to biliary complications as well as eventual graft loss both in the early and late post-operative periods (18). Etiologies of HAS may include allograft rejection, microvascular injury associated with the cold preservation of the liver, or a disrupted vasa vasorum (18–20). Vascular clamp injuries, differences between donor and recipient vessel calibers as well as extrinsic compression, may also lead to HAS (18–20). However, the use of surgical loupes at time of transplantation has been shown to reduce operative time and provide superior patency compared with performing the arterial anastomosis under a surgical microscope (21). Low intra-operative hepatic artery and portal vein flow at the time of transplant also correlates with an increased risk for anastomotic stenosis (22). Interestingly, patients with a presumed underlying immunologic basis for their orthotopic liver transplantation (OLT), such as autoimmune hepatitis, primary biliary cirrhosis, or primary sclerosing cholangitis, do not show a significantly increased risk for postOLT HAS (18).
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Hepatic artery pseudoaneurysm
Hepatic artery pseudoaneurysms most commonly result from surgical manipulation of the hepatic artery or surrounding structures. Additionally, HAPs have been described secondary to salvage procedures related to thrombolysis and angioplasty for hepatic artery stenosis (23, 24). Risk factors for the development of intrahepatic HAPs are interventional procedures such as liver biopsy, percutaneous transhepatic cholangiography, and the placement of transhepatic drainage catheters, while the most important risk factor for extrahepatic HAP is local sepsis (25). Although HAPs may remain asymptomatic and are usually found serendipitously on ultrasound examinations performed post-transplantation, they have potentially severe consequences, such as rupture with consequent hemobilia and intraperitoneal hemorrhage (23, 24, 26). Hepatic artery thrombosis
Hepatic artery thrombosis is categorized by the timing of the event post-transplantation, either as early in the post-operative phase or late. Early HAT refers to thrombosis occurring within two months after liver transplantation (27), whereas late HAT occurs beyond this two-month window. HAT is associated with acute rejection, positive cytomegalovirus serology in the donor, polytransfusion, the use of aortic conduits, variant arterial anatomy, as well as unmatched vessel caliber between the donor and recipient (27–29). Additionally, cold ischemia and prolonged operative times have been linked to HAT following liver transplantation (27–29). Roux-en-Y biliary reconstruction, graft revision, and reoperation are also identified risk factors (28). Graft ischemia in liver transplant recipients caused by HAS and/or HAT contributes significantly to mortality and graft loss after liver transplantation (18, 27, 30, 31). Treatment approaches
There are currently two major therapeutic options for the treatment of these arterial complications: endovascular interventions and surgery (11, 31, 32). The former includes intra-arterial thrombolysis, embolization, percutaneous transluminal angioplasty (PTA), and stent placement. The latter includes thrombectomy, anastomotic reconstruction, and retransplantation. While surgical intervention is often considered the first choice for the management of early HACs, advances in endovascular interventions may make these modalities an acceptable alternative option in many instances.
Arterial complications after liver transplant Hepatic artery anastomotic stricture
Surgical options for the treatment of HAS include resection of the stenotic segment with reanastomosis, aortic conduit graft, interposition vein graft, vein patch angioplasty, or interposition artery graft (18). Revision of the hepatic artery (HA) may help prevent biliary strictures and allow for good long-term graft function in the majority of patients (18). In a previous study, post-revisional HA patency was demonstrated in 78% of cases with revised hepatic arterial anastomoses, and the actuarial patient and graft survivals at four yr were 65% and 56%, respectively (18). Table 1 shows the outcomes of HAS treated by endovascular interventions and surgery in previous studies. The literature supports that endovascular treatment can be successfully performed for HAS and decreases the need for surgical revascularization and liver retransplantation (Fig. 1). The reported PTA and stent placement were safely performed three d to 68 months after liver transplant (Table 1). A study using ultrasound to evaluate the patency of HA demonstrated that both PTA and stent placement can improve HA peak systolic velocity and resistive indices on ultrasound images in HAS patients (33). The primary patency rates after primary stent placement were reported as 92%, 85%, and 69% at one, three, and six months, respectively, compared with 70%, 60%, and 50% after PTA (34). Initial use of a stent may improve primary patency whencomparedwithPTA (35,36). Hepatic artery anastomotic stenosis recurrence is sometimes encountered in patients after transluminal interventional therapy for thrombosis and HAS. Repeated endovascular treatments for recurring HASs have been shown feasible with a high
technical success rate (94.6% hepatic artery patency) and contributed to favorable long-term results (87.7% patient survival in five yr) (19). Nevertheless, endovascular treatment may be unsuccessful in some HAS patients, and to date, this patient population cannot be predicted. Surgical therapy is indicated in such situations. PerezSaborido et al. reported four HAS cases of whom three patients were unsuccessfully treated by percutaneous angioplasty with stent placement. Surgical treatments were then effectively performed in these three patients (5). Hepatic artery pseudoaneurysm
Arteriography should be performed in suspected cases of HAP and is the examination of choice to plan further treatment (25). Coil embolization can be used emergently to achieve hemostasis in unstable patients presenting with pseudoaneurysm rupture, but the resultant hepatic artery occlusion may lead to subsequent graft ischemia (37, 38). Superselective embolization techniques in patients with intrahepatic HAP allow preservation of arterial supply to the graft, with no adverse effect on graft function (25). The small caliber of hepatic arteries initially made stent placement challenging due to the lack of available commercially produced stents; however, the remodeling ability of modern balloon-expandable covered stent grafts has recently been shown to allow adequate exclusion of the pseudoaneurysm and preserve flow in patients with HAP (39) (Fig. 2). Table 2 shows the outcomes of HAP treated by endovascular interventions and surgery in previous studies (40–42). Both hepatic artery ligation and embolization, used as a temporary measure for control of acute
Table 1. Hepatic artery stenosis treated by endovascular interventions and surgery in previous studies
Author (year)
n
Timing from transplant
Frongillo (2013) (15) Hamby (2013) (33) rez-Saborido (2011) (5) Pe kova (2010) (34) La stovic Maruzzelli (2010) (35) da Silva (2008) (20) Huang (2006) (36) Abbasoglu (1997) (18)
10 23 3 19 24 8 14 41
10 m/1–24 m 92.5 d/12–236 d Not reported 2.7 m/3 d–6 m 15.8 m/5–58 m 14.2 m/9–68 m 3-225 d 100/1–1220 d
Management (n) PTA + Stent (10) PTA (10), Stent (13) Surgical treatment (3) PTA + Stent (15), PTA (4) PTA (13), Stent (11) Stent (6), PTA (2) Stent (14) Reanastomosis (17), aortohepatic iliac artery graft (11), interposition vein graft (4), vein patch angioplasty (2), interposition artery graft (1), PTA (6)
Immediate technical success 100% 97.1% 100% 100% 96% 88.9% 85.7% 78% in total, 100% in PTA
Required reintervention, retransplantation or revascularization Not reported 43.5% 0% 15.8% 29.2% 50% 7.1% 17.9%
d, days; m, months; PTA, percutaneous transluminal angioplasty.
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A
B
A
D
Fig. 1. Hepatic artery anastomotic stricture following liver transplantation. (A) Digital subtraction angiography revealing high-grade hepatic arterial anastomotic stricture (arrow) in a 61-yr-old patient post-liver transplantation and (B) its resolution following stent placement across the stenosis (arrow).
B
E
C
F
hemorrhage, can facilitate subsequent successful retransplantation (23, 25). Given surgical revascularization or retransplantation for HAP may be associated with a high mortality rate of up to 69% (25), surgical management is reserved for more complicated cases and indicated when endovascular techniques fail (37, 38). Hepatic arterial thrombosis
Early HAT may lead to graft ischemia and biliary necrosis and is associated with significant graft loss and mortality (27). It was reported that graft survivals were 79% vs. 71% and 50% vs. 50% at one and three yr, respectively, for early HAT and late HAT (43). Because arterial collateralization takes between three wk and four months following arterial thrombosis, graft salvage depends on early detection, limiting warm ischemia and urgent revascularization (8). Therefore, early identification and treatment is critical to recover blood flow
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Fig. 2. Hepatic artery pseudoaneurysm following liver transplantation. (A) Color Doppler ultrasound revealing a large pseudoaneurysm with high turbulent flow in a 50-yr-old patient post-liver transplantation. Select axial (B) and coronal (C) images from CT angiogram confirming a large hepatic arterial anastomotic pseudoaneurysm (arrows). Digital subtraction angiography (D) further delineates the anastomotic pseudoaneurysm (arrow) without involvement of the right or left hepatic artery and (E) its exclusion following covered stent placement across the pseudoaneurysm (arrow). (F) Coronal MIP on follow-up CT angiogram demonstrating stent patency and exclusion of the pseudoaneurysm (arrow).
to rescue the graft. Doppler ultrasonography examination performed at 24 and 48 hr after transplantation can be used as a screening protocol for the early diagnosis of HAT (31). Magnetic resonance angiography (MRA) complements Doppler ultrasound to exclude significant hepatic artery stenosis (44). Computer tomography angiography (CTA) is highly accurate in identifying hepatic artery thrombosis after liver transplantation (45). Treatment of HAT usually requires a surgical intervention including immediate liver retransplantation; however, this option is limited by organ availability (28). Table 3 shows the outcomes of HAT treated by endovascular interventions and surgery in previous studies. Vrochides et al. reported that mean graft survival of 24 HAT patients treated by surgical thrombectomy and arterial reanastomosis was 48.8 months and mean patient survival was 101.2 months (46). Urgent revascularization in cases of early HAT may decrease graft loss, especially when within
Arterial complications after liver transplant Table 2. Hepatic artery pseudoaneurysm treated by endovascular interventions and surgery
Author (year)
n
Timing from transplant
Saad (2013) (37) Chen (2012) (40) Lu (2012) (39) Ou (2010) (41) Ginat (2009) (24) Jones (2008) (16)
12 1 1 1 1 1
157 d/1–1098 d 1d 6m 45 d Not reported 2 wk
Fistouris (2006) (23)
9
39.5 d/14 d–5 yr
Banga (2005) (42) Marshall (2001) (39)
2 11
Lowell (1999) (26)
7 wk, 15 m 30 d/8–132 d
2
Not reported(1), 4 m (1)
Management (n) Embolization (4), Stent (8) Embolization (1) Stent (1) Embolization (1) Stent (1) Embolization followed by surgical excision (1) Surgical excision (3), retransplantation (4), ligation (2) Stent (2) Embolization (6), ligation (3), excision (1), revascularization (1) Surgical reconstruction followed by PTA (1), Surgical repair (1)
Immediate technical success (%)
Normal hepatic flow by ultrasound (%, follow-up time)
83.3% 100% 100% 100% 100% 100%
70% (4.9 m/0-18 m) Not reported 100% (5 m) 100% (6 m) 100% (6 m) 100% (6 wk)
100%
100% in 5 patients from 1996 to 2005 (4.2 yr/7.4 m–6.9 yr)
100% 100%
100% (15 d, 3 yr) Not reported
100%
100% (24 m, 21 m)
d, days; wk, week; m, months; yr, years; PTA, percutaneous transluminal angioplasty.
Table 3. Hepatic artery thrombosis treated by endovascular interventions and surgery
Author (year)
n
Timing from transplant
Intervention (n)
Outcome (follow-up time)
Mali (2012) (8) Grodzicki (2011) (31)
4 23
0 d–1 m Not reported
Retransplant (3), Thrombectomy (1) Retransplant (17), Endovascular (6)
rez-Saborido (2011) (5) Pe Wu (2011) (17)
7 14
Not reported 10/1–41 d
Singhal (2010) (48) Vrochides (2010) (46)
1 24
1d Not reported
Kim (2006) (49) Pinna (1996) (50)
2 17
6 and 4 hr 11 d
Retransplant (6), Surgical aortic graft (1) Rearterialization (3), rearterialization and IA thrombolysis (3), IA thrombolysis (2), Retransplant (6) IA thrombolysis (1) Thrombectomy and arterial reanastomosis at the same site (n = 10), at a different site (n = 14) IA thrombolysis (2) Revascularization (10), Revascularization followed by IA thrombolysis (7)
100% alive (not reported) 64.7% alive (not reported), 50% alive, 50% Retransplant (not reported) 85.7% alive (not reported) 58.3% alive (18-66 m), 50% alive (18-66 m)
100% alive (17.5 m) Mean graft survival was 48.8 m
100% alive (7 m, 8 m) 64.7% alive (17 m)
h, hours; d, days; m, month; IA, intra-arterial.
the first week after liver transplant (43). A previous study revealed that graft salvage may achieve 81% when the revascularization was performed within the first week after liver transplant while late revascularization was unsuccessful in all cases (43). Although survival of HAT patients remains high, this recent study verified the necessity of retransplantation whenever the diagnosis of HAT is confirmed, as surgical thrombectomy and anastomotic revision failed to improve graft survival in eight of 24 patients (46). UNOS/ OPTN policy 3.6 (October 13, 2013) allows for the urgent relisting of liver transplant candidates with HAT within seven d of transplantation as
status 1 with evidence of severe liver injury defined as AST ≥ 3000 and one or both of the following INR ≥ 2.5, acidosis defined as arterial pH ≤ 7.30 or venous pH of 7.25 and/or Lactate ≥ 4 mmol/L. For liver transplant, recipients within 14 d of transplantation with a diagnosis of HAT and not meeting the above criteria are listed with a MELD of 40. This policy reflects the understanding that early and acute onset of HAT post-liver transplantation represents a significant cause of mortality and graft loss while late onset HAT may not necessarily need retransplantation secondary to the development of collaterals (47).
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Although surgical revascularization has traditionally been first-line treatment for early HAT, endovascular interventions are rapidly evolving and have recently achieved high success rates (13, 30, 35). If suspicion exists for an arterial complication by ultrasound, the diagnosis should be confirmed by arteriography and, if possible, treatment should be attempted by fibrinolysis, angioplasty, or even stent placement for graft salvage (5). Local thrombolysis can also be used to treat acute HAT occurring immediately after stent deployment (Fig. 3) (35). HAS is a contributor to HAT; however, percutaneous transluminal angioplasty of focal HAS can reduce the incidence of HAT more than threefold (30). Conclusions and future directions
With the evolution of endovascular techniques and improved angioplasty and stent technology, many complications of liver transplant that were traditionally treated surgically may be addressed by an endovascular approach. Endovascular treatment is less invasive than surgical intervention and harbors good overall results; however, surgery should be available in the event endovascular techniques are unsuccessful or not feasible. With respect to HAS, further study is needed into what, if any, features of the patient or lesion will help predict those patients that would benefit
A
B
C
D
E
F
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most from endovascular therapy. Determining these factors is crucial to managing these patients and triaging them to angioplasty or stenting or going directly to surgical revision. There is evidence that primarily stenting these lesions may yield a longer primary patency vs. angioplasty alone. Comparing covered vs. uncovered stents, the potential effectiveness of drug eluting stents or angioplasty with drug eluting balloons are possible areas for future study. Covered stenting is often preferable to surgery in patients with HAP due to a significant mortality rate associated with surgical intervention. Angiography is also important for confirmation of the diagnosis and rapid control of the hepatic artery in cases of pseudoaneurysm rupture. For patients with HAT, Doppler ultrasound shows good sensitivity and specificity in early detection of arterial thrombosis. Arteriography can confirm the diagnosis and select patients for intervention. Of course, rapid restoration of blood flow is a priority in these patients by surgical or endovascular means. Catheter-directed thrombolysis with possible angioplasty and/or stenting has been successfully employed to treat HAT and is an area for future exploration. Continued research to identify the patient factors and lesion characteristics of those patients that would benefit from endovascular revascularization vs. surgery may change the paradigm for treatment of this serious post-transplant complication.
Fig. 3. Hepatic artery stenosis and thrombosis following liver transplantation. (A) Digital subtraction angiography revealing high-grade focal hepatic arterial anastomotic stricture (arrow) in a 57-yr-old patient post-liver transplantation and (B) improved flow following angioplasty at the stenosis (arrow). (C) Subsequent arterial thrombosis apparent on postangioplasty angiography (arrow). (D) Minimal improvement in thrombosis after intra-arterial administration of tPA (arrow). Axial (E) and (F) coronal CT images showing subsequent biloma formation (arrow) after hepatic artery thrombosis, ultimately requiring retransplant.
Arterial complications after liver transplant Vascular complications following liver transplant remain a significant source of morbidity and cause of graft loss requiring retransplantation. Hepatic arterial complications are the most commonly encountered of these vascular complications. Expedient management is imperative for graft salvage. The development of endovascular interventions for managing these complications has added to the armamentarium with good overall success. Improving our understanding of the patient characteristics or surgical techniques that place patients at risk for these complications may avoid or reduce these complications and, in turn, improve patient survival. References 1. MURRAY KF, CARITHERS RL Jr; AASLD. AASLD practice guidelines: evaluation of the patient for liver transplantation. Hepatology 2005: 41: 1407. 2. SCHUPPAN D, AFDHAL NH. Liver cirrhosis. Lancet 2008: 371: 838. 3. MOON DB, LEE SG. Liver transplantation. Gut Liver 2009: 3: 145. 4. DECAENS T. Liver transplantation for hepatocellular carcinoma: time for an international consensus. Clin Res Hepatol Gastroenterol 2012: 36: 316. -SABORIDO B, PACHECO-SANCHEZ D, BARRERA-REBOL5. PEREZ LO A et al. Incidence, management, and results of vascular complications after liver transplantation. Transplant Proc 2011: 43: 749. € K, ENNE M, FERNANDES R et al. Vascular 6. STEINBRUCK complications after living donor liver transplantation: a Brazilian, single-center experience. Transplant Proc 2011: 43: 196. 7. SINTRA SN, TOME L, CIPRIANO MA, BENTO C, FURTADO E. Long-term outcome of the first 150 liver transplant recipients: a single-center experience. Transplant Proc 2013: 45: 1119. 8. MALI VP, AW M, QUAK SH, LOH DL, PRABHAKARAN K. Vascular complications in pediatric liver transplantation; single-center experience from Singapore. Transplant Proc 2012: 44: 1373. 9. MESQUITA MC, FERREIRA AR, VELOSO LF et al. Pediatric liver transplantation: 10 years of experience at a single center in Brazil. J Pediatr (Rio J) 2008: 84: 395. 10. HEFFRON TG, PILLEN T, WELCH D, SMALLWOOD GA, REDD D, ROMERO R. Hepatic artery thrombosis in pediatric liver transplantation. Transplant Proc 2003: 35: 1447. 11. WAKIYA T, SANADA Y, MIZUTA K et al. A comparison of open surgery and endovascular intervention for hepatic artery complications after pediatric liver transplantation. Transplant Proc 2013: 45: 323. 12. BOYVAT F, AYTEKIN C, KARAKAYALI H, HABERAL M. Interventional radiology in liver transplant. Exp Clin Transplant 2008: 6: 105. 13. KARANI JB, YU DF, KANE PA. Interventional radiology in liver transplantation. Cardiovasc Intervent Radiol 2005: 28: 271. 14. AZZAM AZ, TANAKA K. Management of vascular complications after living donor liver transplantation. Hepatogastroenterology 2012: 59: 182. 15. FRONGILLO F, GROSSI U, LIROSI MC et al. Incidence, management, and results of hepatic artery stenosis after liver
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