- Email: [email protected]
Portal Vein Thrombosis in Patients Undergoing Orthotopic Liver Transplantation: Intraoperative Endovascular Radiological Procedures
Portal Vein Thrombosis in Patients Undergoing Orthotopic Liver Transplantation: Intraoperative Endovascular Radiological Procedures M. Gómez-Gutierrez, J. Quintela, M. Marini, B. Gala, F. Suarez, I. Cao, C.C. Sellés, J. Aguirrezabalaga, A. Otero, and S. Mosteiro ABSTRACT Purpose. To evaluate the usefulness of endovascular procedures for portal vein complications during orthotopic liver transplantation (OLT). Materials and methods. Between May 1994 and November 2004, we performed 504 OLTs in 464 adults. Seventy-eight patients (16.8%) presented with portal vein thrombosis (PVT). This analysis of patients from May 2000 to September 2004 included 10 patients with PVT, who were treated with endovascular techniques due to low portal flow. We compared this group with patients who were treated surgically with attention to rethrombosis and survival rates. If portal vein problems were due to obstruction, a venoplasty and primary stent placement were performed. We also embolized with coils or surgically ligated remaining competitive portosystemic shunts. Results. Perfusion problems in the allograft were solved in all cases. We placed seven stents and embolized six competitive shunts. One anastomotic dysfunction was repaired. None of the patients died or rethrombosed during surgery or follow-up. Conclusion. Endovascular techniques during OLT can resolve some liver graft perfusion problems due to PVT and “steal” phenomena, especially with unsatisfactory eversion thromboendovenectomy in patients with grade IV PVT. Although primary permeability of stents has been good, these results need to be confirmed.
P
ORTAL VEIN THROMBOSIS (PVT) is a frequent complication among patients undergoing orthotopic liver transplantation (OLT); it continues to have a substantial impact on surgical complexity and perioperative morbidity and mortality rates.1–5 Endovascular techniques are a safe, effective treatment of vascular complications.6 –9 However, it is unusual to require combined cooperation between surgeons and interventional radiologists during OLT. The aim of this work was to present our experience in intraoperative treatment of PVT and closure of competitive shunts by means of endovascular techniques during OLT. We compared rethromboses and patient survival rates between patients with PVT treated by operative management and those treated with endovascular techniques. MATERIALS AND METHODS Our hospital performed 504 OLTs in 464 adults between May 1994 and November 2004. Seventy-eight patients (16.8%) presented with PVT at the time of OLT. PVT extension was classified as four grades1: grade I, n ⫽ 14/17.9%; grade II, n ⫽ 26/33.3%; grade III, n ⫽ 22/28.2%; and grade IV, n ⫽ 15/19.2%. The study group of 10
patients with PVT, grade III and IV, treated with endovascular techniques was obtained from May 2000 to September 2004. We compared this cohort with those displaying PVT grade III and IV who underwent surgical techniques for rethrombosis and survival rates. The surgical technique was eversion thromboendovenectomy2– 4 with an end-to-end portal vein anastomosis. If the portal flow was insufficient, an interventional radiologist was called into the operating theatre to perform portography and endovascular treatment. Portography, pressure gradients, and endovascular treatments were taken either via the graft umbilical vein (UV) or via one of the recipient mesenteric vein tributaries. If the cause of sluggish flow was an obstructive or incomplete thrombus removal, a venoplasty followed by primary placement of a 14 ⫻ 30-mm Wallstent was performed. Next, we embolized with multiple 10- to From the Department of Radiology (M.M., I.C., S.M.) and Liver Transplant Unit (M.G.-G., J.Q., B.G., F.S., C.C.S., J.A., A.O.), Hospital Juan Canalejo, La Coruña, Spain. Address reprints request to Milagros Marini, MD, Department of Radiology, Hospital Universitario Juan Canalejo, Xubias de arriba, 84 La Coruña 15006, Spain. E-mail: milagros_marini@ canalejo.org
0041-1345/05/$–see front matter doi:10.1016/j.transproceed.2005.10.063
© 2005 by Elsevier Inc. All rights reserved. 360 Park Avenue South, New York, NY 10010-1710
3906
Transplantation Proceedings, 37, 3906 –3908 (2005)
PORTAL VEIN THROMBOSIS
3907
Table 1. Summary of Patient Clinical Characteristics and Endovascular Treatment of Extensive Chronic Splanchnic Vein Thrombosis During Liver Transplantation Patient no.
Cause of OLT
OLT date
Grade of PVT
Endovascular procedure
Complications
Follow-up 11/31/2004
1 2
Alcohol ⫹ HCC Criptogenic
05/07/2000 06/26/2000
IV III
None None
Alive Alive
3 4 5 6 7 8 9 10
Alcohol ⫹ HCC Alcohol ⫹ HCC Alcohol ⫹ HCC Alcohol ⫹ HCC Alcohol Regraft VHC HBV ⫹ Sugiura
11/02/2000 01/10/2002 09/05/2002 11/26/2002 01/29/2003 11/02/2003 01/04/2004 01/30/2004
IV III III III III IV III IV
Stent ⫹ shunt embolization Anastomotic dysfunction ⫹ shunt embolization Stent ⫹ shunt embolization Shunt embolizations Stent ⫹ shunt embolization Stent ⫹ shunt embolization Stent Stent Surgical collateral ligations Stent
None None None None None None None None
Alive Alive Alive Alive Alive Alive Alive Alive
HCC, hepatocellular carcinoma; HCV, hepatitis C virus; HBV, hepatitis B virus.
15-mm diameter coils, and we surgically ligated any remaining competitive portosystemic shunts. Once suitable results had been obtained, the surgical team completed the OLT. Patients were not anticoagulated either during the endovascular procedure or in the postoperative period, nor were antiplatelet agents used routinely during follow-up. Follow-up included Doppler ultrasound assessment of PV patency (Table 1). Student t test and the chi-square test were used to compare means and proportions between the groups. The Kaplan-Meier product limit estimation was used to calculate patient survival. A P value of ⬍.05 was considered significant.
RESULTS
Our series included four cases of grade IV PVT (surgical control group n ⫽ 11) and six cases of grade III PVT (surgical group control n ⫽ 16). Portal recanalization, primary stent placement, and closure of competitive shunts were successful in all patients. Portal perfusion in the allograft was adequate. Portal hypertension resolved in all patients and no complications were observed during the endovascular procedure. None of the patients died during surgery or in the early or late postoperative or follow-up periods (mean follow-up 25.6 months; range 8 to 54; Table 1). No rethrombosis has been observed in the endovasculartreated group, whereas in grade IV PVT patients undergoing only surgical treatment, seven patients (63,6%) experienced a postoperative rethrombosis and two patients, a late rethrombosis (P ⫽ .014). The postoperative mortality rate for this group was 57% (n ⫽ 4) (P ⫽ .04). Lastly, in grade III PVT patients undergoing only surgical treatment, one patient had a postoperative rethrombosis (treated by means of a bypass) and two patients had a late rethombosis (P ⫽ .012). There were no related deaths in these patients. DISCUSSION
Currently there is no consensus about the most suitable surgical approach to treat PVT during OLT. Despite the introduction of alternative techniques, the operative mortality rates remain high (9.1% to 42%).1– 4 The major risk is the recurrence of PVT. Prognosis is poor in the event of
rethrombosis, particularly in the early posttransplantation period.1– 4 Portal recanalization and reconstruction with endovascular stents are established, effective radiological procedures to treat PVT.6 – 8 In all our cases, portography proved to be useful to identify unsuspected preoperative PVT (patients 1 through 3). Portogram afforded a precise identification of an occluded or a partially removed thrombus in the recipient portal system (patients 1, 3, 8, 10), of anastomotic dysfunction (patients 2, 5, 6), and of steal phenomena due to native portosystemic communications (patients 1 through 6, 9; Table 1). Because patients had already undergone incomplete thromboendovenectomy, which is regarded by some authors as a technique with a high risk of rethrombosis, we placed a primary stent to prevent rethrombosis. The longterm permeability of stents has not been clearly established.6 –9 The most important factors in portal vein stent occlusion are liver disease and/or obstruction of the splanchnic veins.10 All patients received a new liver graft. The blood flow in the occluded veins was improved by placing stents and embolizing any vessels involved in steal phenomena,11,12 which may be the reason why follow-up showed 100% primary permeability. To conclude, although surgical techniques resolve the majority of PVT cases, stent placement in the splenomesentericportal veins and closure of competitive shunts via endovascular techniques during OLT is a safe, and effective procedure to solve liver graft perfusion due to PVT and steal phenomena. In complex cases of splenomesenteric PVT (grade IV), operating theatre cooperation between surgeons and interventional radiologists enhances patient therapeutic options. Although primary permeability of stents upon medium- and long-term follow-up has been good, the results reported here need to be confirmed in future studies.
REFERENCES 1. Stieber AC, Zetti G, Todo S, et al: The spectrum of portal vein thrombosis in liver transplantation. Ann Surg 213:199, 1990
3908 2. Lerut JP, Mazza D, Leeuw VV, et al: Adult liver transplantation and abnormalities of splanchnic veins: experience in 53 patients. Transpl Int 10:125, 1997 3. Yerdel MA, Gunson B, Mirza D, et al: Portal vein thrombosis in adults undergoing liver transplantation: risk factors, screening, management, and outcome. Transplantation 69:1873, 2000 4. Molmenti EP, Roodhouse TW, Molmenti H, et al: Thrombendvenectomy for organized portal vein thrombosis at the time of liver transplantation. Ann Surg 235:292, 2002 5. Nonami T, Yokoyama I, Iwatsuki S, et al: The incidence of portal vein thrombosis at liver transplantation. Hepatology 16: 1195, 1992 6. Zajko AB, Sheng R, Bron K, et al: Percutaneous transluminal angioplasty of venous anastomotic stenoses complicating liver transplantation: intermediate-term results. J Vasc Interv Radiol 5:121, 1994 7. Cherukuri R, Haskal ZJ, Naji A, et al: Percutaneous thrombolysis and stent placement for the treatment of portal vein
GÓMEZ-GUTIERREZ, QUINTELA, MARINI ET AL thrombosis after liver transplantation: long-term follow-up. Transplantation 65:1124, 1998 8. Funaki B, Jordan D, Rosenblum JD, et al: Percutaneous treatment of portal venous stenosis in children and adolescents with segmental hepatic transplants: long-term results. Radiology 215:147, 2000 9. Lee SY, Koo GY, Gwon DY, et al: Living donor liver transplantation: complications in donors and interventional management. Radiology 230:443, 2004 10. Stein M, Link DP: Symptomatic spleno-mesenteric.portal venous thrombosis: recanalization and reconstruction with endovascular stents. J Vasc Interv Radiol 10:363, 1999 11. Durham JD, LaBerge JM, Altman S, et al: Portal vein thrombolysis and closure of competitive shunts following liver transplantation. J Vasc Interv Radiol 5:611, 1994 12. Bilbao JI, Arias M, Herrero JI, et al: Percutaneous transhepatic treatment of a posttransplant portal vein thrombosis and a preexisting spontaneous splenorenal shunt. Cardiovasc Intervent Radiol 18:323, 1995
P
ORTAL VEIN THROMBOSIS (PVT) is a frequent complication among patients undergoing orthotopic liver transplantation (OLT); it continues to have a substantial impact on surgical complexity and perioperative morbidity and mortality rates.1–5 Endovascular techniques are a safe, effective treatment of vascular complications.6 –9 However, it is unusual to require combined cooperation between surgeons and interventional radiologists during OLT. The aim of this work was to present our experience in intraoperative treatment of PVT and closure of competitive shunts by means of endovascular techniques during OLT. We compared rethromboses and patient survival rates between patients with PVT treated by operative management and those treated with endovascular techniques. MATERIALS AND METHODS Our hospital performed 504 OLTs in 464 adults between May 1994 and November 2004. Seventy-eight patients (16.8%) presented with PVT at the time of OLT. PVT extension was classified as four grades1: grade I, n ⫽ 14/17.9%; grade II, n ⫽ 26/33.3%; grade III, n ⫽ 22/28.2%; and grade IV, n ⫽ 15/19.2%. The study group of 10
patients with PVT, grade III and IV, treated with endovascular techniques was obtained from May 2000 to September 2004. We compared this cohort with those displaying PVT grade III and IV who underwent surgical techniques for rethrombosis and survival rates. The surgical technique was eversion thromboendovenectomy2– 4 with an end-to-end portal vein anastomosis. If the portal flow was insufficient, an interventional radiologist was called into the operating theatre to perform portography and endovascular treatment. Portography, pressure gradients, and endovascular treatments were taken either via the graft umbilical vein (UV) or via one of the recipient mesenteric vein tributaries. If the cause of sluggish flow was an obstructive or incomplete thrombus removal, a venoplasty followed by primary placement of a 14 ⫻ 30-mm Wallstent was performed. Next, we embolized with multiple 10- to From the Department of Radiology (M.M., I.C., S.M.) and Liver Transplant Unit (M.G.-G., J.Q., B.G., F.S., C.C.S., J.A., A.O.), Hospital Juan Canalejo, La Coruña, Spain. Address reprints request to Milagros Marini, MD, Department of Radiology, Hospital Universitario Juan Canalejo, Xubias de arriba, 84 La Coruña 15006, Spain. E-mail: milagros_marini@ canalejo.org
0041-1345/05/$–see front matter doi:10.1016/j.transproceed.2005.10.063
© 2005 by Elsevier Inc. All rights reserved. 360 Park Avenue South, New York, NY 10010-1710
3906
Transplantation Proceedings, 37, 3906 –3908 (2005)
PORTAL VEIN THROMBOSIS
3907
Table 1. Summary of Patient Clinical Characteristics and Endovascular Treatment of Extensive Chronic Splanchnic Vein Thrombosis During Liver Transplantation Patient no.
Cause of OLT
OLT date
Grade of PVT
Endovascular procedure
Complications
Follow-up 11/31/2004
1 2
Alcohol ⫹ HCC Criptogenic
05/07/2000 06/26/2000
IV III
None None
Alive Alive
3 4 5 6 7 8 9 10
Alcohol ⫹ HCC Alcohol ⫹ HCC Alcohol ⫹ HCC Alcohol ⫹ HCC Alcohol Regraft VHC HBV ⫹ Sugiura
11/02/2000 01/10/2002 09/05/2002 11/26/2002 01/29/2003 11/02/2003 01/04/2004 01/30/2004
IV III III III III IV III IV
Stent ⫹ shunt embolization Anastomotic dysfunction ⫹ shunt embolization Stent ⫹ shunt embolization Shunt embolizations Stent ⫹ shunt embolization Stent ⫹ shunt embolization Stent Stent Surgical collateral ligations Stent
None None None None None None None None
Alive Alive Alive Alive Alive Alive Alive Alive
HCC, hepatocellular carcinoma; HCV, hepatitis C virus; HBV, hepatitis B virus.
15-mm diameter coils, and we surgically ligated any remaining competitive portosystemic shunts. Once suitable results had been obtained, the surgical team completed the OLT. Patients were not anticoagulated either during the endovascular procedure or in the postoperative period, nor were antiplatelet agents used routinely during follow-up. Follow-up included Doppler ultrasound assessment of PV patency (Table 1). Student t test and the chi-square test were used to compare means and proportions between the groups. The Kaplan-Meier product limit estimation was used to calculate patient survival. A P value of ⬍.05 was considered significant.
RESULTS
Our series included four cases of grade IV PVT (surgical control group n ⫽ 11) and six cases of grade III PVT (surgical group control n ⫽ 16). Portal recanalization, primary stent placement, and closure of competitive shunts were successful in all patients. Portal perfusion in the allograft was adequate. Portal hypertension resolved in all patients and no complications were observed during the endovascular procedure. None of the patients died during surgery or in the early or late postoperative or follow-up periods (mean follow-up 25.6 months; range 8 to 54; Table 1). No rethrombosis has been observed in the endovasculartreated group, whereas in grade IV PVT patients undergoing only surgical treatment, seven patients (63,6%) experienced a postoperative rethrombosis and two patients, a late rethrombosis (P ⫽ .014). The postoperative mortality rate for this group was 57% (n ⫽ 4) (P ⫽ .04). Lastly, in grade III PVT patients undergoing only surgical treatment, one patient had a postoperative rethrombosis (treated by means of a bypass) and two patients had a late rethombosis (P ⫽ .012). There were no related deaths in these patients. DISCUSSION
Currently there is no consensus about the most suitable surgical approach to treat PVT during OLT. Despite the introduction of alternative techniques, the operative mortality rates remain high (9.1% to 42%).1– 4 The major risk is the recurrence of PVT. Prognosis is poor in the event of
rethrombosis, particularly in the early posttransplantation period.1– 4 Portal recanalization and reconstruction with endovascular stents are established, effective radiological procedures to treat PVT.6 – 8 In all our cases, portography proved to be useful to identify unsuspected preoperative PVT (patients 1 through 3). Portogram afforded a precise identification of an occluded or a partially removed thrombus in the recipient portal system (patients 1, 3, 8, 10), of anastomotic dysfunction (patients 2, 5, 6), and of steal phenomena due to native portosystemic communications (patients 1 through 6, 9; Table 1). Because patients had already undergone incomplete thromboendovenectomy, which is regarded by some authors as a technique with a high risk of rethrombosis, we placed a primary stent to prevent rethrombosis. The longterm permeability of stents has not been clearly established.6 –9 The most important factors in portal vein stent occlusion are liver disease and/or obstruction of the splanchnic veins.10 All patients received a new liver graft. The blood flow in the occluded veins was improved by placing stents and embolizing any vessels involved in steal phenomena,11,12 which may be the reason why follow-up showed 100% primary permeability. To conclude, although surgical techniques resolve the majority of PVT cases, stent placement in the splenomesentericportal veins and closure of competitive shunts via endovascular techniques during OLT is a safe, and effective procedure to solve liver graft perfusion due to PVT and steal phenomena. In complex cases of splenomesenteric PVT (grade IV), operating theatre cooperation between surgeons and interventional radiologists enhances patient therapeutic options. Although primary permeability of stents upon medium- and long-term follow-up has been good, the results reported here need to be confirmed in future studies.
REFERENCES 1. Stieber AC, Zetti G, Todo S, et al: The spectrum of portal vein thrombosis in liver transplantation. Ann Surg 213:199, 1990
3908 2. Lerut JP, Mazza D, Leeuw VV, et al: Adult liver transplantation and abnormalities of splanchnic veins: experience in 53 patients. Transpl Int 10:125, 1997 3. Yerdel MA, Gunson B, Mirza D, et al: Portal vein thrombosis in adults undergoing liver transplantation: risk factors, screening, management, and outcome. Transplantation 69:1873, 2000 4. Molmenti EP, Roodhouse TW, Molmenti H, et al: Thrombendvenectomy for organized portal vein thrombosis at the time of liver transplantation. Ann Surg 235:292, 2002 5. Nonami T, Yokoyama I, Iwatsuki S, et al: The incidence of portal vein thrombosis at liver transplantation. Hepatology 16: 1195, 1992 6. Zajko AB, Sheng R, Bron K, et al: Percutaneous transluminal angioplasty of venous anastomotic stenoses complicating liver transplantation: intermediate-term results. J Vasc Interv Radiol 5:121, 1994 7. Cherukuri R, Haskal ZJ, Naji A, et al: Percutaneous thrombolysis and stent placement for the treatment of portal vein
GÓMEZ-GUTIERREZ, QUINTELA, MARINI ET AL thrombosis after liver transplantation: long-term follow-up. Transplantation 65:1124, 1998 8. Funaki B, Jordan D, Rosenblum JD, et al: Percutaneous treatment of portal venous stenosis in children and adolescents with segmental hepatic transplants: long-term results. Radiology 215:147, 2000 9. Lee SY, Koo GY, Gwon DY, et al: Living donor liver transplantation: complications in donors and interventional management. Radiology 230:443, 2004 10. Stein M, Link DP: Symptomatic spleno-mesenteric.portal venous thrombosis: recanalization and reconstruction with endovascular stents. J Vasc Interv Radiol 10:363, 1999 11. Durham JD, LaBerge JM, Altman S, et al: Portal vein thrombolysis and closure of competitive shunts following liver transplantation. J Vasc Interv Radiol 5:611, 1994 12. Bilbao JI, Arias M, Herrero JI, et al: Percutaneous transhepatic treatment of a posttransplant portal vein thrombosis and a preexisting spontaneous splenorenal shunt. Cardiovasc Intervent Radiol 18:323, 1995