LIVER TRANSPLANTATION 21:944–952, 2015
ORIGINAL ARTICLE
The Friendly Incidental Portal Vein Thrombus in Liver Transplantation Peng Soon Koh, See Ching Chan, Kenneth Siu-Ho Chok, William Wei Sharr, Tiffany Cho-Lam Wong, Sui Ling Sin, and Chung Mau Lo Division of Liver Transplantation, Department of Surgery, Queen Mary Hospital, The University of Hong Kong, Hong Kong
Improved outcomes have been shown in liver transplantation (LT) with portal vein thrombosis (PVT). However, PVT is still discovered incidentally during surgery despite careful preoperative imaging. Data are limited comparing the outcomes of incidental PVT with PVT diagnosed via preoperative imaging before LT. This study aims to compare the overall outcomes of patients with PVT. From 2008 to 2012, 369 patients had LT, and 58 patients with PVT were identified. They were divided into those with non-PVT (group 0; n 5 311), preoperatively identified PVT (group 1; n 5 28), and incidental PVT (group 2; n 5 30). The demographics, characteristics, preoperative assessment, and postoperative outcomes were compared. A survival analysis was also performed. Baseline characteristics and preoperative evaluations of all 3 groups were comparable (P > 0.05) except for Model for End-Stage Liver Disease score, tumor status, platelet levels, and serum bilirubin. A multivariate analysis only showed a high serum bilirubin level to be a predictor of PVT (P 5 0.004; odds ratio, 3.395; 95% confidence interval, 1.467-7.861). Postoperative outcomes were also comparable (P > 0.05). Compared to group 2, group 1 had more patients with a Yerdel classification of 3 or 4 with more extensive surgical intervention required (P 5 0.02). The survival analysis in all 3 groups was comparable with 5-year survival rate of 87.4%, 84.6%, and 91.8% in group 0, 1, and 2, respectively (P 5 0.66). In conclusion, recipients with PVT undergoing LT can have similar outcomes as the non-PVT patients even if PVTs were discovered incidentally. Discovery of incidental PVT only requires thrombectomy with no substantial change of treatment strategy, and the outcome is not adversely affected because most incidental PVTs are of a lower Yerdel grade. Preoperative imaging is useful to identify those with a higher Yerdel grade to allow planning of surgical strategy during transC 2015 AASLD. plantation. Liver Transpl 21:944-952, 2015. V Received December 7, 2014; accepted April 12, 2015. Recent studies have shown that portal vein thrombosis (PVT) is feasible in liver transplantation (LT) compared to the past, where it was once considered a contraindication because of technical difficulty and was associated with a high mortality and morbidity. The early era of PVT management in LT showed significant mortality and morbidity. However, with improved surgical techniques, technical capabilities, and surgical innovations, we have seen a marked
improvement in the management of PVT with lower mortality and morbidity as shown in recently published data.1,2 The incidence of PVT has been reported to be approximately 2%-26% in various studies.3,4 Therefore, a good preoperative plan and strategy for identifying patients undergoing LT with PVT are vital to ensure good perioperative outcome and long-term consequences. Despite careful preoperative planning
Abbreviations: CT, computed tomography; DDLT, deceased donor liver transplantation; HCC, hepatocellular carcinoma; HV, hepatic vein; INR, international normalized ratio; IVC, inferior vena cava; LDLT, living donor liver transplantation; LT, liver transplantation; MELD, Model for End-Stage Liver Disease; OR, odds ratio; OS, overall survival; PTLD, posttransplant lymphoproliferative disease; PV, portal vein; PVT, portal vein thrombosis; SMV, superior mesenteric vein; U/S, ultrasound. Funding sources: Nothing to report. Potential conflict of interest: Nothing to report. Address reprint requests to See Ching Chan, M.B.B.S., M.S., Ph.D., M.D., F.R.C.S. (Edin), F.H.K.A.M. (Surg), F.A.C.S., Division of Liver Transplantation, Department of Surgery, Queen Mary Hospital, The University of Hong Kong, Pok Fu Lam Road, Hong Kong. Telephone: 1852 2255 3025; FAX: 1852 2817 5475; E-mail: [email protected] or [email protected] DOI 10.1002/lt.24149 View this article online at wileyonlinelibrary.com. LIVER TRANSPLANTATION.DOI 10.1002/lt. Published on behalf of the American Association for the Study of Liver Diseases
C 2015 American Association for the Study of Liver Diseases. V
LIVER TRANSPLANTATION, Vol. 21, No. 7, 2015
with the various imaging techniques that are available, PVT is at times discovered incidentally during surgery and hence, may affect the operative strategy and outcome.5 Since there are limited data to date comparing the outcome of PVT when encountered incidentally during the intraoperative period with PVT diagnosed before surgery by preoperative imaging, this study aims to compare the overall outcomes of patients with PVT in these 2 groups based on data from a center with decades of experience in LT.
PATIENTS AND METHODS Patient Selection From January 2008 to December 2012, there were 369 patients who underwent LT at the Department of Surgery, Queen Mary Hospital, The University of Hong Kong. Among these patients, 182 (49.3%) patients had deceased donor liver transplantation (DDLT) and 187 (50.7%) patients had living donor liver transplantation (LDLT). Analyses were performed in those who were diagnosed with PVT during LT from our prospectively collected data. PVT is usually not a contraindication for LT in our center. Recipients with PVT usually had conventional thrombectomy performed with some having to undergo a thromboendovenectomy or an interposition graft. A flowmeter using the Transonic Flow-QC (Transonic Systems, Inc., Ithaca, NY) is usually used to measure portal vein flow after PVT removal to ensure adequate portal flow with a portal venography performed via the inferior mesenteric vein occasionally. All patients undergoing LT will have standard radiological imaging before transplantation. The commonly used modality for imaging was a contrast-enhanced computed tomography scan, and a few of the patients had transabdominal ultrasound or magnetic resonance imaging as part of their workup. All patients who were diagnosed with evidence of PVT during radiological imaging were included in the study and defined as group 1. Patients with no evidence of PVT noted during radiological imaging but who were intraoperatively found to have PVT were included as well; this group of patients was defined as those with “incidental” PVT or group 2. For comparative reasons, the remaining patients with no PVT were known as group 0.
Classifying on the Basis of the Yerdel Classification The standard classification of PVT commonly used is the Yerdel classification according to the extent of thrombosis and is described as follows: grade 1, minimally or partially thrombosed portal vein in which the thrombosed area is mild or at the most confined to 50% occlusion of the portal vein (PV), including total occlusions, with or without minimal extension into the SMV; grade 3, complete thrombosis
KOH ET AL. 945
of both PV and proximal SMV, whereas distal SMV is open; and grade 4, complete thrombosis of the PV and proximal as well as distal SMV.2 In this study where incidental PVT was also identified, Yerdel grades 1 and 2 were classed together for comparative reasons because it was difficult to distinguish between these 2 grades intraoperatively.
Outcome Measurement, Statistical Analysis, and Overall Survival (OS) Analysis The baseline characteristics and demographics of patients undergoing transplantation between groups 1 and 2 as well as the group with no PVT were compared. The preoperative, intraoperative, and postoperative variables along with the type of management undertaken were analyzed and compared. Also, patient and graft survival analyses were also performed. Categorical variables were compared using Pearson chi-square or Fisher’s exact test when appropriate. Continuous variables were expressed as median with range and were compared using a Kruskal-Wallis test. The likelihood of developing PVT based on patients’ characteristics was also determined by a multivariate analysis by the logistic regression method and expressed as an odds ratio (OR) with a 95% confidence interval (CI). The Kaplan-Meier method was performed for both groups where the 1-, 3-, and 5-year OS was determined for both patient and graft survival. Further comparison of OS between the groups was performed with the log-rank test. Statistical analysis was performed using SPSS, version 21.0 (IBM, Armonk, NY), and a P value of
ORIGINAL ARTICLE
The Friendly Incidental Portal Vein Thrombus in Liver Transplantation Peng Soon Koh, See Ching Chan, Kenneth Siu-Ho Chok, William Wei Sharr, Tiffany Cho-Lam Wong, Sui Ling Sin, and Chung Mau Lo Division of Liver Transplantation, Department of Surgery, Queen Mary Hospital, The University of Hong Kong, Hong Kong
Improved outcomes have been shown in liver transplantation (LT) with portal vein thrombosis (PVT). However, PVT is still discovered incidentally during surgery despite careful preoperative imaging. Data are limited comparing the outcomes of incidental PVT with PVT diagnosed via preoperative imaging before LT. This study aims to compare the overall outcomes of patients with PVT. From 2008 to 2012, 369 patients had LT, and 58 patients with PVT were identified. They were divided into those with non-PVT (group 0; n 5 311), preoperatively identified PVT (group 1; n 5 28), and incidental PVT (group 2; n 5 30). The demographics, characteristics, preoperative assessment, and postoperative outcomes were compared. A survival analysis was also performed. Baseline characteristics and preoperative evaluations of all 3 groups were comparable (P > 0.05) except for Model for End-Stage Liver Disease score, tumor status, platelet levels, and serum bilirubin. A multivariate analysis only showed a high serum bilirubin level to be a predictor of PVT (P 5 0.004; odds ratio, 3.395; 95% confidence interval, 1.467-7.861). Postoperative outcomes were also comparable (P > 0.05). Compared to group 2, group 1 had more patients with a Yerdel classification of 3 or 4 with more extensive surgical intervention required (P 5 0.02). The survival analysis in all 3 groups was comparable with 5-year survival rate of 87.4%, 84.6%, and 91.8% in group 0, 1, and 2, respectively (P 5 0.66). In conclusion, recipients with PVT undergoing LT can have similar outcomes as the non-PVT patients even if PVTs were discovered incidentally. Discovery of incidental PVT only requires thrombectomy with no substantial change of treatment strategy, and the outcome is not adversely affected because most incidental PVTs are of a lower Yerdel grade. Preoperative imaging is useful to identify those with a higher Yerdel grade to allow planning of surgical strategy during transC 2015 AASLD. plantation. Liver Transpl 21:944-952, 2015. V Received December 7, 2014; accepted April 12, 2015. Recent studies have shown that portal vein thrombosis (PVT) is feasible in liver transplantation (LT) compared to the past, where it was once considered a contraindication because of technical difficulty and was associated with a high mortality and morbidity. The early era of PVT management in LT showed significant mortality and morbidity. However, with improved surgical techniques, technical capabilities, and surgical innovations, we have seen a marked
improvement in the management of PVT with lower mortality and morbidity as shown in recently published data.1,2 The incidence of PVT has been reported to be approximately 2%-26% in various studies.3,4 Therefore, a good preoperative plan and strategy for identifying patients undergoing LT with PVT are vital to ensure good perioperative outcome and long-term consequences. Despite careful preoperative planning
Abbreviations: CT, computed tomography; DDLT, deceased donor liver transplantation; HCC, hepatocellular carcinoma; HV, hepatic vein; INR, international normalized ratio; IVC, inferior vena cava; LDLT, living donor liver transplantation; LT, liver transplantation; MELD, Model for End-Stage Liver Disease; OR, odds ratio; OS, overall survival; PTLD, posttransplant lymphoproliferative disease; PV, portal vein; PVT, portal vein thrombosis; SMV, superior mesenteric vein; U/S, ultrasound. Funding sources: Nothing to report. Potential conflict of interest: Nothing to report. Address reprint requests to See Ching Chan, M.B.B.S., M.S., Ph.D., M.D., F.R.C.S. (Edin), F.H.K.A.M. (Surg), F.A.C.S., Division of Liver Transplantation, Department of Surgery, Queen Mary Hospital, The University of Hong Kong, Pok Fu Lam Road, Hong Kong. Telephone: 1852 2255 3025; FAX: 1852 2817 5475; E-mail: [email protected] or [email protected] DOI 10.1002/lt.24149 View this article online at wileyonlinelibrary.com. LIVER TRANSPLANTATION.DOI 10.1002/lt. Published on behalf of the American Association for the Study of Liver Diseases
C 2015 American Association for the Study of Liver Diseases. V
LIVER TRANSPLANTATION, Vol. 21, No. 7, 2015
with the various imaging techniques that are available, PVT is at times discovered incidentally during surgery and hence, may affect the operative strategy and outcome.5 Since there are limited data to date comparing the outcome of PVT when encountered incidentally during the intraoperative period with PVT diagnosed before surgery by preoperative imaging, this study aims to compare the overall outcomes of patients with PVT in these 2 groups based on data from a center with decades of experience in LT.
PATIENTS AND METHODS Patient Selection From January 2008 to December 2012, there were 369 patients who underwent LT at the Department of Surgery, Queen Mary Hospital, The University of Hong Kong. Among these patients, 182 (49.3%) patients had deceased donor liver transplantation (DDLT) and 187 (50.7%) patients had living donor liver transplantation (LDLT). Analyses were performed in those who were diagnosed with PVT during LT from our prospectively collected data. PVT is usually not a contraindication for LT in our center. Recipients with PVT usually had conventional thrombectomy performed with some having to undergo a thromboendovenectomy or an interposition graft. A flowmeter using the Transonic Flow-QC (Transonic Systems, Inc., Ithaca, NY) is usually used to measure portal vein flow after PVT removal to ensure adequate portal flow with a portal venography performed via the inferior mesenteric vein occasionally. All patients undergoing LT will have standard radiological imaging before transplantation. The commonly used modality for imaging was a contrast-enhanced computed tomography scan, and a few of the patients had transabdominal ultrasound or magnetic resonance imaging as part of their workup. All patients who were diagnosed with evidence of PVT during radiological imaging were included in the study and defined as group 1. Patients with no evidence of PVT noted during radiological imaging but who were intraoperatively found to have PVT were included as well; this group of patients was defined as those with “incidental” PVT or group 2. For comparative reasons, the remaining patients with no PVT were known as group 0.
Classifying on the Basis of the Yerdel Classification The standard classification of PVT commonly used is the Yerdel classification according to the extent of thrombosis and is described as follows: grade 1, minimally or partially thrombosed portal vein in which the thrombosed area is mild or at the most confined to 50% occlusion of the portal vein (PV), including total occlusions, with or without minimal extension into the SMV; grade 3, complete thrombosis
KOH ET AL. 945
of both PV and proximal SMV, whereas distal SMV is open; and grade 4, complete thrombosis of the PV and proximal as well as distal SMV.2 In this study where incidental PVT was also identified, Yerdel grades 1 and 2 were classed together for comparative reasons because it was difficult to distinguish between these 2 grades intraoperatively.
Outcome Measurement, Statistical Analysis, and Overall Survival (OS) Analysis The baseline characteristics and demographics of patients undergoing transplantation between groups 1 and 2 as well as the group with no PVT were compared. The preoperative, intraoperative, and postoperative variables along with the type of management undertaken were analyzed and compared. Also, patient and graft survival analyses were also performed. Categorical variables were compared using Pearson chi-square or Fisher’s exact test when appropriate. Continuous variables were expressed as median with range and were compared using a Kruskal-Wallis test. The likelihood of developing PVT based on patients’ characteristics was also determined by a multivariate analysis by the logistic regression method and expressed as an odds ratio (OR) with a 95% confidence interval (CI). The Kaplan-Meier method was performed for both groups where the 1-, 3-, and 5-year OS was determined for both patient and graft survival. Further comparison of OS between the groups was performed with the log-rank test. Statistical analysis was performed using SPSS, version 21.0 (IBM, Armonk, NY), and a P value of
