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Yi NJ, Suh KS, Kim T, et al. Current role of surgery in treatment of early stage hepatocellular carcinoma: resection versus liver transplantation. Oncology 2008; 75(Suppl 1): 124. Poon RT, Fan ST, Lo CM, et al. Long-term survival and pattern of recurrence after resection of small hepatocellular carcinoma in patients with preserved liver function: implications for a strategy of salvage transplantation. Ann Surg 2002; 235: 373. Adam R, Azoulay D, Castaing D, et al. Liver resection as a bridge to transplantation for hepatocellular carcinoma on cirrhosis: a reasonable strategy? Ann Surg 2003; 238: 508. Park MS, Lee KW, Suh SW, et al. Liver Transplantation Versus Liver Resection for the Treatment of Hepatocellular Carcinoma. Liver Transpl 2013; 19(Suppl 1 (6)): S118. Suh KS, Cho EH, Lee HW, et al. Liver transplantation for hepatocellular carcinoma in patients who do not meet the Milan criteria. Dig Dis 2007; 25: 329. Yang SH, Suh KS, Lee HW, et al. A revised scoring system utilizing serum alphafetoprotein levels to expand candidates for living donor transplantation in hepatocellular carcinoma. Surgery 2007; 141: 598. Lee JW, Paeng JC, Kang KW, et al. Prediction of tumor recurrence by 18F-FDG PET in liver transplantation for hepatocellular carcinoma. J Nucl Med 2009; 50: 682. Hong G, Suh KS, Kim HY, et al. Preoperative serum AFP level and serum PIVKA II level and 18F-FDG PET positivity of the tumor predict tumor recurrence better than Milan criteria for patients with HCC in adult-to-adult living donor liver transplantation. Liver Transpl 2012; 18(Suppl 1): S94. Elsharkawi M, Staib L, Henne-Bruns D, et al. Complete remission of postransplant lung metastases from hepatocellular carcinoma under therapy with sirolimus and mycophenolate mofetil. Transplantation 2005; 79: 855. Kornberg A, Kupper B, Tannapfel A, et al. Long-term survival after recurrent hepatocellular carcinoma in liver transplant patients: clinical patterns and outcome variables. Eur J Surg Oncol 2010; 36: 275. Suh KS, Hong G, Kim HY, et al. Outcome of living donor liver transplantation for patients with far advanced hepatocellular carcinoma. Liver Transpl 2012; 18(Suppl 1): S214.
SECTION 6. MANAGEMENT OF EXTENSIVE NONTUMOROUS PORTAL VEIN THROMBOSIS IN ADULT LIVING DONOR LIVER TRANSPLANTATION
Deok-Bog Moon,1 Sung-Gyu Lee,1,2 Chul-Soo Ahn,1 Shin Hwang,1 Ki-Hun Kim,1 Tae-Yong Ha,1 Gi-Won Song,1 Dong-Hwan Jung,1 Gil-Chun Park,1 Jung-Man Namkoong,1 Hyung-Woo Park,1 Yo-Han Park,1 Cheon-Soo Park,1 Kyu-Bo Sung,1 Gi-Young Ko,1 and Dong-Il Gwon1 Background. Patent portal vein (PV) and adequate portal inflow is essential for successful living donor liver transplantation (LDLT). In extensive portal vein thrombosis (PVT) patients, however, complete PV thrombectomy is not feasible particularly at intrapancreatic portion, and subsequently portal flow steal through preexisting sizable collaterals or rethrombosis can occur. To overcome those problems, we introduced interruption of sizable collaterals and intraoperative cine-portogram (IOP), which is useful for diagnosis and treatment of residual PVT and sizable collaterals. Methods. Fourteen percent of adult LDLT (188/1399) had PVT from February 2008 to December 2012 and were subdivided into
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Yerdel’s grades 1, 2, 3, and 4 based on preoperative imaging and operative findings. Considering the severity of PVT and presence of sizable collaterals, the managements were as follows: thrombectomy alone, additional PV plasty, PV stenting, interposition graft, or additional interruption of collaterals. Results. The Yerdel’s grade of PVT patients were 1 (42%), 2 (54%), 3 (3%), and 4 (1%). One hundred one (77%) patients underwent interruption of sizable collaterals. The most common management for PVT was thrombectomy alone in grades 1 and 2, thrombectomy plus PV stenting and/or ballooning in grade 3, and interposition graft in grade 4. In LDLT for PVT patients, 1-year mortality was 9%, and PV-related complication occurred in 5%. The severity of PVT made no difference in the outcome. Conclusion. Multi-disciplinary approaches including surgical correction of PVT, IOP, and interruption of sizable collaterals resulted in excellent outcome, and it was not affected by the severity of PVT. Keywords: Portal vein thrombosis, Adult, Living donor liver transplantation, Management.
eceased donor liver transplantation (DDLT) in patients with portal vein thrombosis (PVT) is no longer considered a contraindication at most centers because of surgical innovations (1Y5). In living donor liver transplantation (LDLT), the management is principally similar to DDLT, but the issue of subjecting a healthy donor to potentially significant morbidity and mortality has led to a critical reassessment of some of the recipient selection criteria that are considered acceptable in DDLT (6). Moreover, based on the greater technical difficulties and the results obtained from DDLT in extensive PVT patients including complete thrombosis of main PV, Yerdel grades 3 and 4 patients, presence of extensive PVT in the recipient has often been considered to be a relative or absolute contraindication in LDLT (7). The scarcity of DDLT in Korea, however, led us to perform ceaseless trials to tackle the extensive PVT in LDLT at our institution and the recent outcomes are not inferior to DDLT for PVT patients. To be a successful LDLT for PVT patient, we have to give a special consideration to the anatomies of both donor’s PV and recipient’s portosplanchnic venous system. In regard to donor PV, it has relatively small diameter corresponding to recipient main PV and short of length compared to deceased whole organ donor. Variant PV anatomy, such as type II or III PV, posterior PV arising from main PV, is also common. There are limited resources of a fresh deceased donor venous conduit for extra-anatomic PV anastomosis. In regard to recipient PV, the diameter of PV
D
The authors declare no funding or conflicts of interest. 1 Division of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Korea. 2 Address correspondence to: Sung-Gyu Lee, M.D., F.A.C.S., Division of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, 388-1 Pungnap-dong, Songpa-gu, Seoul 138-736, Korea. E-mail: [email protected] S.-G.L. and D.-B.M. participated in research design. S.-G.L., D.-B.M., C.-S.A. participated in writing of the paper. S.-G.L., D.-B.M., S.H., K.-H.K., T.-Y.H., G.-W.S., D.-H.J., G.-C.P., K.-B.S., G.-Y.K., D.-I.G. participated in performance of the research. J.-M.N., H.-W.P. contributed new reagents or analytic tools. Y.-H.P. and C.-S.P. participated in data analysis.
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is often too small for donor PV because of combined PV stenosis related to chronic organized thrombus, and also sometimes inversely too large after thrombectomy. The quality of recipient PV wall is often poor and paper thin from trauma during dissection and thrombectomy. In case of dual-graft LDLT, right and left PV bifurcations need to be preserved for reconstruction of PVs of both implanting grafts. Complete thrombectomy of extensive PVT during transplantation is often not secured, particularly, at intrapancreatic PV segment, and we should take care of coexistent sizable portosystemic collaterals, which might be the cause of portal flow steal and PV rethrombosis and result in failure of the implanted partial liver graft. To overcome those problems, we introduced interruption of sizable collaterals and intraoperative cine-portogram (IOP) during adult LDLT, which is useful tool for diagnosis and treatment of residual PVT and sizable collaterals. In this article, we described that how to apply our novel approaches for extensive PVT patients and the outcomes of adult LDLT for PVT patients at our institution.
MATERIALS AND METHODS From February 2008 through December 2012, a total of 1679 adult patients underwent liver transplantation (LT) consisting of 1399 cases of LDLT and 280 cases of DDLT at Asan Medical Center, Seoul, Korea. When we exclude the patients who had tumor-related PVT confirmed pathologically, a total number of nontumorous PVT patients were 223 patients (13.3%) consisting of 188 cases (14.4%) of LDLT and 35 cases (12.5%) of DDLT. Both Doppler ultrasound and 3-dimensional computed tomography (3DCT) scans were performed in all patients within 1 month before LT. Based on the degree and extent of PVT-assessed preoperative Doppler ultrasound and 3DCT scan, PVT was classified into four grades (Yerdel grading), that is, grade 1: the PV minimally or partially thrombosed, less than 50% of the vessel lumen; grade 2: more than 50% occlusion of the PV including total occlusion; grade 3: complete thrombosis of both PV and proximal superior mesenteric vein (SMV); and grade 4: complete thrombosis of the PV as well as proximal and distal SMV (5). In addition, we arbitrarily classified PVT patients into two groups in consideration of difficulty in surgical technique and simplicity of comparison, that is, partial PVT: less than 90% occlusion of the PV; complete PVT: 90% to 100% near complete occlusion of the PV. They included 173 male and 50 female patients with a median age of 54 years (range 18 Y 70). The original disease, their Child-Turcotte-Pugh classification, the Model for End-Stage Liver Disease (MELD) score, and preoperative complications are shown in Table 1.
SURGICAL TECHNIQUES PVT can result in development of numerous minute or sizable pericholedochal varix and cumbersome bleeding may occur during dissection of hepatic hilum. In addition, PV thrombectomy is one of the most critical procedures, and time consuming PV plasty is often necessary. As a result, dissection of hepatic hilum is performed as a last procedure after completion of another hepatectomy procedure. When the large collateral veins functioning main splanchnic venous outflow are used for portal inflow vessel in form of end-to-end anastomosis such as left renal vein (LRV) draining large splenorenal shunt (SRS), or when large amount of ascites are present in the absence of large collateral veins, indicating unrelieved severe portal hypertension, venovenous bypass of the splanchnic blood flow through the interposition graft to decompress portal hypertension is useful for avoiding bowel congestion and also reduction of bleeding.
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Most of grade 1 PVT can be managed by low dissection and eversion thrombectomy with end-to-end donor-recipient portal anastomosis. Some of grade 2 and 3 PVT can also be resolved with thrombectomy. However, although portal blood flow look like full restoration, complete thrombectomy, not leaving remnant PVT and/or stenosis, is not feasible in many grades 2 and 3 patients, particularly at intrapancreatic segment of PV. Furthermore, sizable portosystemic collaterals often coexist with residual PVT (Fig. 1). Therefore, we evaluate portal blood flow from the divided PV stump after thrombectomy and also before and after interruption of sizable portosystemic collaterals to decide whether the thrombectomized PV can be adequate portal inflow to the liver graft or not. If recipient’s PV is inadequate for portal inflow, interposition graft is employed from SMVor LRV of patient with large spontaneous splenorenal shunt (SRS). When recipient’s PV was decided to use for portal inflow, measurement of its luminal diameter was performed. If the PV diameter, expected to anastomose to the graft PV, is less than 1 cm after thrombectomy, we perform PV plasty with autologous bisected great saphenous vein (GSV) to enlarge its diameter and avoid anastomotic stricture because PV diameter should be at least 1 cm diameter to relieve PV stenosis and also to effectively decompress portal hypertension by virtue of our experiences. If recipient’s PV has too large and thick wall after thrombectomy in contrast to the graft PV with small and thin wall, we perform funnel-shape fencing to the graft PV with bisected GSV at the back-table for adjustment of graft PV to the recipient’s PV and anastomosis without difficulty (Fig. 2). In addition, surgical interruption of sizable collaterals is held after engraftment and perfusion to give adequate portal flow into the graft. In case of grade 4 PVT, when there is a suitable large splanchnic collateral vein satisfying at least 1 cm size in diameter such as coronary vein, inferior mesenteric vein, LRV in case of splenorenal shunt, SMV branch or pericholedochal vein, it can be used as a portal inflow vessel by interposition graft during adult LDLT. When pericholedochal vein is
TABLE 1. Demographic data of patients with portal vein thrombosis (PVT) Original disease Liver cirrhosis without HCC Liver cirrhosis with HCC Autoimmune hepatitis Idiopathic portal vein thrombosis Portal bilopathy Wilson’s disease Congenital hepatic fibrosis Biliary atresia Preoperative condition Child-Turcoote-Pugh classifications (A/B/C) MELD score Below 15/ 15j25 / above 25 Ascities (no / controlled / uncontrolled) Gastrointestinal bleeding (no / yes) Encephalopathy (no / yes)
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No. 136 80 3 1 1 1 1 1 29 / 78 / 116 21.2T7.6 96 / 90 / 37 20 / 120 / 83 105 / 118 123 / 100
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FIGURE 1. A, Preoperative 3-dimensional computed tomography (3D-CT) revealed complete portal vein thrombosis (PVT) and large coronary vein and splenorenal shunt draining into left renal vein, which drained most of splanchnic blood flow in A1 and 2. Intraoperative cine-portogram (IOP) showed no residual PVT after thrombectomy and disappearance of portosystemic collaterals after ligation of coronary vein in A3. B, Preoperative 3D-CT revealed complete PVT extended in proximal superior mesenteric vein and large coronary vein in A1 and 2. IOP after PVT thrombectomy showed residual PVT at the intrapancreatic PV and proximal SMV and portal flow steal through persistent large coronary vein in B3.
present in form of less than 1 cm sized small multiple veins, pericholedochal vein is usually inadequate for portal inflow vessel because of technical difficulties and little possibility of effective routes for portal decompression. In the absence of a suitable collateral vein, there is still no effective solution in adult LDLT, although portocaval hemitransposition has been advocated in DDLT or pediatric LDLT (8, 9). When artificial ringed polytetrafluoroethylene (PTFE) vascular graft was necessary as an interposition graft in the absence of available fresh cadaveric vessel, vascular fence using bisected GSV was intervened between the both ends of ringed PTFE graft and collateral vein and donor PV respectively to avoid disastrous event from the disparities of their diameter and vessel wall conditions, as described by ours (10).
APPLICATION OF IOP We initiated the IOP during LDLT on March 2003 to overcome the limitations of intraoperative Doppler ultrasound that had been used to estimate the adequacy of portal inflow (11, 12). The IOP can be performed not only in LDLT but also in DDLT to precisely visualize the significant spontaneous portosystemic collaterals not detected by intraoperative Doppler ultrasound, and monitor the completeness of collateral ligation. In addition, it can be a useful treatment tool for remained PVT or stenosis and surgically uninterrupted sizable collaterals through PV stenting (Wallstent, Boston Scientific or Zilver stent, Cook) and coil embolization of collaterals respectively. The stent are made of Nitinol shape-memory alloy consisting nikel and titanium. There might be a possibility of re-thrombosis after stenting in terms of long-term follow-up, and all the patients who underwent PV stenting are treated with Coumadin. The
target of prothrombin time (INR) is 1.5Y2.5. However, rethrombosis rarely occur during early period of portal venous stenting if large portosystemic collateral vessels are effectively interrupted and all the splanchnic venous flow goes into the liver graft through PV on IOP. It can be performed through inferior mesenteric vein or superior mesenteric branches under fluoroscope. During IOP, we should obtained two types of portograms including SMV and splenic vein (SV) portogram respectively in order to visualize the whole splanchnic venous system (Fig. 3). After PV thrombectomy for grades 1, 2, and some of 3, we perform IOP to evaluate whether PVT is completely removed or not. Based on IOP, we perform PV stenting or additional ballooning when the luminal diameter is less than 1 cm, or the degree of luminal narrowing is more than 50% of cross-section area despite maintenance of more than 1 cm luminal diameter. When more than 1 cm luminal diameter is maintained at the remained thrombus level without floating thrombus and portal flow steal is absent, additional treatment is usually not necessary. For some of grades 3 and 4 patients with sizable collaterals who needs jump graft for portal vein reconstruction, we sometimes perform IOP after laparotomy to decide the best portal inflow vessel among the several possible splanchnic veins or collaterals and also to decide appropriate interruption site for avoidance of portal flow steal.
RESULTS Among 223 patients with PVT, 211 patients (94.6%) were diagnosed preoperatively. Twelve patients (5.4%) were diagnosed during the transplant procedure, but all the patient belonged grade 1 and additional management except thrombectomy was not necessary. Based on occlusive grade
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FIGURE 2. A, Preoperative 3-dimensional computed tomography (3D-CT) revealed complete portal vein thrombosis (PVT) extended into proximal superior mesenteric vein (SMV) in A1. The portal vein (PV) diameter was measured more than 2 cm in A2, and we performed funnel-shape fencing to the graft PV with bisected great saphenous vein (GSV) such at the back-table as schema of A3 for easy and safe anastomosis with large recipient’s PV. A4 is completion view, and white arrowhead indicate GSV fence intervening between donor PV and recipient’s PV indicated by white arrow. B, Preoperative 3D-CT revealed obliterated PV with chronic organized PVT and large coronary vein in B1. Eversion PV thrombectomy was performed in B2 and PV plasty with bisected GSV was performed to enlarge PV diameter more than 1 cm in B3. B4 is the completion view of PV reconstruction showing no stenosis at the suprapancreatic PV.
of PV, 77% (171/223) had partial PVT, and 23.3% (52/223) had complete PVT. According to Yerdel grade, 93 had grade 1 (42%), 120 grade 2 (54%), 7 grade 3 (3%), and 3 grade 4 (1%). One hundred seventy-one patients (77%) had sizable portosystemic collaterals and needed surgical interruption and/or coil embolization during IOP for maintenance of adequate portal blood flow without portal flow steal.
Table 2 shows the operative management of PVT between partial PVT and complete PVT. In partial PVT, thrombectomy only (54%, 93/171) was the most common surgical procedure. In complete PVT, however, thrombectomy and PV stenting and/or ballooning under IOP (33%, 17/52) was the most common management. PV plasty to correct PV stenosis related to chronic organized PVT was
FIGURE 3. Intraoperative portogram (IOP) was checked after engraftment. Both superior mesenteric vein portogram (A) and splenic vein portogram should be checked to visualize the whole splanchnic venous system.
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TABLE 2. Management of portal vein thrombosis (PVT) during liver transplantation Methods Thrombectomy Thrombectomy and PV plasty Thrombectomy and PV plasty and PV stenting and/or ballooning Thrombectomy and PV stenting and/or ballooning Interposition graft Choledochal varix-portal anastomosis
Partial (n=171)
Complete (n=52)
93 (54%) 17 (10%) 20 (12%)
10 (19%) 3 (6%) 9 (17%)
41 (24%)
17 (33%)
0 0
12# (23%) 1 (2%)
Abbreviations: PV, portal vein. # Portal inflow of the 12 interposition grafts consisted of 6 left renal vein, 3 superior mesenteric vein, 1 inferior mesenteric vein, 1 coronary vein, 1 mesenteric collateral vein.
necessary in 22% (37/171) of partial PVT and 23% (12/52) of complete PVT. The portal inflow vessels used for interposition jump graft were the left renal vein (renoportal anastomosis) (50%, 6/12), SMV (25%, 3/12), inferior mesenteric vein, coronary vein, and mesenteric collaterals in 1 patient, respectively. The operative management according to Yerdel grade as followings. Grade1 consisted of thrombectomy only (67%, 62/93), thrombectomy and PV stenting and/or ballooning (20%, 19/93), thrombectomy and PV plasty (12%, 11/93), and additional PV stenting (1%, 1/93). Grade 2 consisted of thrombectomy only (34%, 41/120), thrombectomy and PV stenting and/or ballooning (28%, 34/120), thrombectomy and PV plasty with stenting (23%, 28/120), and interposition jump graft (7%, 8/120). Grade 3 consisted of thrombectomy and PV plasty with stenting (71%, 5/7) and interposition jump graft (29%, 2/7). Grade 4 consisted of interposition jump graft (67%, 2/3) and choledochal varix-PV anastomosis (33%, 1/3). The overall incidence of PVT related complication is 4.9% (11/223), and it consisted of PV stenosis (45%, 5/11), TABLE 3.
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rethrombosis (18%, 2/11), PV tearing (18%, 2/11), and portal flow steal related graft dysfunction (18%, 2/11). PV stenosis and rethrombosis did not occur in patients who underwent PV stenting but in patients who underwent PV thrombectomy only. PV tearing developed from PV stenting into relatively small PV with paper-thin wall in one patient, and from PV ballooning with inadequately large-diameter balloon in another patient. Although surgical ligation of sizable collaterals was performed at the time of PV thrombectomy and stenting, portal flow steal related graft dysfunction occurred in 2 patients because complete evaluation of whole splanchnic venous system on IOP was not held through both SMV and SV portogram and we missed a chance to interrupt residual sizable collaterals. Hospital mortality occurred in five patients (2%, 5/223), and the primary causes were rethrombosis in 2 patients, portal flow steal related graft dysfunction in 2 patients, and PV tearing in 1 patients (Table 3). One patient underwent retransplantation on postoperative days 53 using deceased donor whole liver due to not PV related complication but hepatic artery injury related delayed hepatic arterial thrombosis. He had grade 4 PVT but sizable pericholedochal varix and mesenteric collateral were present. Left hepatic artery (LHA) was the only available arterial inflow in the hepatic hilum because dissection for other hepatic arteries was not possible from copious bleeding and cavernous transformation of hepatic hilum. Intimal detachment of hepatic arterial wall after hilar dissection developed and mural hematoma propagated into the whole celiac arterial system. The overall 1- and 5-year survival rates in PVT patients after LT were 88% and 84%, respectively. The 1- and 5-year survival rates in LDLT were 91% and 87%, and the difference between PVT and non-PVT patients was negligible when compared to previous report (13). The 1-year and 5-year survival rate in DDLT were 69% and 69% respectively, significantly lower survival rate than LDLT. It was not related to management difference but resulted from the poorer preoperative status among DDLT patients (Fig. 4). The 1- and 5-year survival rate after LDLT for PVT patients was not different between partial and complete PVT. Furthermore, Yerdel grades 3 and 4 patients are all alive without
Portal vein related complications after liver transplantation in patients with PVT
No.
PVT
Type of LT
Management of PVT
Complication
Time of complication
Outcome
1 2 3 4 5 6 7 8 9 10 11
Partial Partial Partial Partial Partial Partial Partial Complete Partial Partial Complete
LDLT LDLT LDLT DDLT LDLT LDLT LDLT LDLT LDLT LDLT LDLT
Incomplete thrombectomy Thrombectomy + PV stent Thrombectomy + PV stent Incomplete thrombectomy Thrombectomy only Thrombectomy only Thrombectomy + PV stent Thrombectomy only Thrombectomy only Thrombectomy + ballooning Thrombectomy only
Rethrombosis PV tearing Portal flow steal through LGV Rethrombosis PV stenosis PV stenosis Portal flow steal through IMV PV stenosis PV stenosis) PV rupture PV stenosis
Day 0 Day 0 Day 53 Day 2 10 months Day 14 Day 6 4 months 3 months Day 0 6 months
Dead Dead Dead Dead Alive Alive Dead Alive Alive Alive Alive
Abbreviations: PVT, portal vein thrombosis; LT, liver transplantation; LDLT, living donor liver transplantation; DDLT, deceased donor liver transplantation; PV, portal vein; LGV, left gonadal vein; IMV, inferior mesenteric vein.
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FIGURE 4. Overall patient survival rates in patients with portal vein thrombosis. A, After liver transplantation. B, Comparison between living donor liver transplantation and deceased donor liver transplantation.
PV-related complication, and there is no difference between grades 1 and 2 PVT patients (Fig. 5).
DISCUSSION Preexisting PVT is no more contraindication in DDLT (1Y5), and LDLT for PVT patients also has been performed in some centers (14Y16). Large proportion among extensive PVT patients including complete PVT, or Yerdel grade 3 and 4, however, are excluded from LDLT or the LDLT should be delayed until a DDLT becomes available for an extraanatomic PV reconstruction (15). The plausible explanation is the possibility of extreme difficulty in hilar dissection due to extensive collateral formation and inflammatory changes around the PV (16). For LDLT, recipient PV should be long enough because the graft PV is very short, and the HA should be preserved up to second-order branches to adjust the size and the length because the graft HA is short and small. Dissection of HA without intimal dissection is one of the key procedure to guarantee successful LDLT. As a result, successful completion of the described procedures is very difficult for patients with extensive PVT. At our
institution, however, when we consider LT for PVT patients, the decision for LDLT or DDLT has not been affected by the severity of PVT but by the presence of available donor except grade 4 diffuse portomesenteric thrombosis patients without sizable collaterals that cavo-portal hemitransposition or multivisceral transplantation is the only possible treatment option in the setting of DDLT. The incidence of PVT among LDLT patients at our institution was 14.4%, similar to the incidence in DDLT patients, which was 12.5%. Restoration and maintenance of the normal portal flow is absolutely essential for good graft function and also regeneration of the partial liver graft after LDLT. Hence, we made it a rule to secure luminal diameter of PV at least 1 cm through the whole length and interruption of sizable portosystemic collaterals. For effective thrombectomy during LDLT, dissection of PV from the right and left portal bifurcation to the splenomesenteric confluence level is necessary. However, it is feasible for only a few patients with extensive PVT because access to the intrapancreatic portion of PV is difficult because of high risk of uncontrollable copious bleeding from the preexisting extensive collaterals. At our institution, effective
FIGURE 5. Overall patient survival rate in patients with portal vein thrombosis (PVT) according the severity. A, Comparison between partial and complete PVT. B, Comparison between Yeldel’s grade 1, 2, 3, and 4 PVT.
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thrombectomy that assure normal portal flow was not possible for 33% of grade 1 PVT, 66% of grade 2 PVT, and all the grade 3 and 4 patients. Furthermore, 77% of PVT patients had large portosystemic collaterals on preoperative 3D-CT scan that needed interruption during LT. As a special measure to tackle those problems, we routinely performed IOP during LT for PVT patients and evaluated the completeness of thrombectomy and presence of residual portosystemic collaterals in the splanchnic venous system and also treated them under IOP. As an additional procedure to normalize portal flow after PV thrombectomy, we performed PV plasty to alleviate PV stenosis related with chronic organized PVT in 45% (49/110) among incompletely thrombectomized grade 1 and 2 PVT patients. However, 59% (29/49) of PV plasty patients needed PV stenting additionally to relieve residual PV stenosis at the intrapancreatic PV segment during IOP. Although PV was not stenotic in 73% (156/213) at the suprapancreatic PV segment after PV thrombectomy among grade 1 and 2 PVT patients, 34% (53/156) had residual PVT at the intrapancreatic PV segment and PV stenting was required to maintain luminal diameter of PV. Two third (8/12) of interposition jump graft patients belonged to grade 2 PVT, and 71% (5/7) of grade 3 PVT patients, on the other hand, could be treated by additional PV stenting and/or balloon dilatation under IOP. All the 3 patients of grade 4 PVT at our institution underwent LDLT using large portosystemic collaterals as a portal inflow vessel to establish the portal flow, and IOP was useful to decide which collateral vessels could be used for portal inflow. The necessity for interposition jump graft was decided preoperatively after review of pre-operative 3D-CT scanned within 1 month. The eighty three percent (10/12) of interposition jump graft was performed with LDLT. In the early period, the LDLTs were performed only when fresh cadaveric vessel graft was prepared because the patency rate of cryopreserved vein graft was not satisfactory due to development of aneurysm, thrombosis, stricture (17, 18). Hence, some of recipient candidates requiring interposition jump graft lost opportunity to undergo LT under scarcity of deceased organ donation. Since we successfully performed renoportal anastomosis with ringed-PTFE interposition graft in January 2010, 12 to 16 mm diametered artificial PTFE vascular grafts have been used in all the 9 patients requiring interposition jump graft on LDLT for timely LT without worsening the patient’s condition any more. All patients received low molecular weight heparin for 7 days and vitamin K antagonists (target INR 1.5Y2.0) have been used permanently to prevent foreign body reaction related delayed thrombosis. Until now, all the artificial interposition grafts are patent without thrombosis. At our institution, the 1-year mortality of PVT patients after LDLT was 9%, and the incidence of PV related complication was only 5% (11/223). To our knowledge, it is one of the best outcomes throughout the field of LDLT and DDLT also. It was resulted from the efforts to establish normal portal flow without portal flow steal through combined approaches including surgical managements such as thrombectomy, PV plasty, interruption of large portosystemic collaterals, and interposition jump graft if necessary, and radiologic evaluation for residual PV stenosis, thrombus, and sizable collaterals, and radiologic intervention such as PV stenting and/or ballooning, and coil embolization
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under the guidance of IOP. IOP was an extremely useful tool to tackle the PVT patients during LT, but inadequate application of PV stenting and/or ballooning and incomplete evaluation of splanchnic venous system can result in PV tearing and portal flow steal respectively. The incidence of rethrombosis of the PV was 1% (2/223) and occurred in the early period of this study. Both cases also could have been avoided if we employed IOP appropriately. Considering the 5 cases with delayed development of PV stenosis after PV thrombectomy only, possibly due to slowly progressing periportal inflammatory reaction, we had better perform PV stenting selectively to avoid delayed PV stenosis when PV diameter or residual PV thrombosis marginally escape from the conditions requiring intervention. In LDLT for PVT patients, not only PV-related complications but also hepatic artery (HA)Yrelated complications is prone to develop because HA injury can often occur during dissection of hepatic hilum when pericholedochal varix or cavernous transformation of hepatic hilum is present, and alternative available arterial inflow vessels or interposing fresh cadaveric iliac artery that have small branches corresponding to graft HA are usually absent. Particularly in extensive PVT patients including grades 3 and 4, we have to perform meticulous dissection to reduce HA injury such as direct arterial wall injury or intimal dissection from mural hematoma propagation. Yerdel’s grade for PVT has been considered the most adequate classification because it correlates the thrombosis extension with the surgical technique and outcome (5, 19). In our series, management of grade 4 PVT corresponded to the report, but in case of grades 1, 2, and 3 PVT patients, Yerdel’s classification based on the data in the setting of DDLT was less practical because the management was not decided by Yerdel’s grade but by the degree of suprapancreatic PV stenosis, residual thrombosis or stenosis at intrapancreatic PV segment after thrombectomy, and presence of large portosystemic collaterals on IOP. In case of grade 1 and 2 PVT, additional managements such as PV plasty, PV stenting and/or ballooning, interposition jump graft, and collateral interruption were necessary. In case of grade 3 PVT PV thrombectomy and PV stent and/or ballooning was more common treatment than interposition jump graft. The preoperative 3D-CT scan and IOP finding after PV thrombectomy were key factors to decide appropriate management, and the described treatment strategy made no difference in the outcomes regardless of severity of PVT.
CONCLUSION LDLT for nontumorous PVT patients achieved excellent outcome in our series, but there must be a direct relation to the postoperative mortality. Multidisciplinary approaches including surgical correction of PVT, IOP, and interruption of sizable collaterals decreased PVT-related complications and showed almost same results despite difference of severity of PVT. In contrast to DDLT, total portomesenteric thrombosis without sizable collaterals is still unsettled task in the field of LDLT. ACKNOWLEDGMENTS The authors would like to acknowledge the efforts of Bo-Hyun Jeong, Seong-Hwa Kang, and Young-In Yun.
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SECTION 7. A NEW THERAPEUTIC STRATEGY ON PORTAL FLOW MODULATION THAT INCREASES DONOR SAFETY WITH GOOD RECIPIENT OUTCOMES
Toshimi Kaido,1,3 Kohei Ogawa,1 Yasuhiro Fujimoto,1 Takashi Ito,1 Koji Tomiyama,1 Akira Mori,1 Yasuhiro Ogura,2 and Shinji Uemoto1
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Abstract. The goal of this study was to examine whether the lower limit of the graft-to-recipient weight ratio (GRWR) can be safely reduced to make better use of the left lobe graft in adult-to-adult living donor liver transplantation in combination with portal pressure control. Beginning December 2007, the acceptable limit for GRWR was lowered to Q0.7% and by April 2009, it was further lowered to Q0.6%. A portal pressure control program targeting a final portal pressure G15 mm Hg was also introduced. The donor complication rate decreased from 13.8% to 9.3%. The overall survival of recipients with GRWR G0.8% did not differ from recipients with a GRWR Q0.8%. In conclusion, the lower limit of the GRWR can be safely reduced to 0.6% using a left lobe graft in adult-toadult living donor liver transplantation in combination with portal pressure control. Keywords: Liver transplantation, Portal flow modulation, Graftto-recipient weight ratio, Small-for-size graft.
onor safety and favorable outcomes of recipients after liver transplantation (LT) are the most important priorities of living donor liver transplantation (LDLT). We recently established a new therapeutic strategy to satisfy both priorities. The strategy consists of grafting the left lobe first, decreasing the lower limit of the graft-to-recipient weight ratio (GRWR) and controlling portal pressure. The present short essay describes details and the value of our new strategy.
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GRAFT SELECTION One hundred ninety-two adult (age Q18 years) patients underwent LDLT at Kyoto University Hospital between February 2008 and April 2012. The incidence of all donor complications including donors for pediatric recipients is higher when using right (n=500, 44.2%), compared with left or extended lateral lobe grafts (n=762, 18.8%) (PG0.001) (1). Biliary complications are more frequent after right, than after left or extended lateral lobe grafts (12.2% vs. 4.9%, PG0.001). Thus, left lobe grafts are preferable because of lower complication rates and a larger remnant liver that ensures donor safety. However, the lower limit of GRWR and the risk of small-for-size syndrome are critical problems that need to be overcome when using left lobe grafts. Eight hundred and ten adult recipients underwent LDLT at Kyoto University Hospital between February 1999 and March 2012. We have routinely applied the portal The authors declare no funding or conflicts of interest. 1 Division of Hepato-Biliary-Pancreatic and Transplant Surgery, Department of Surgery, Graduate School of Medicine, Kyoto University, Kyoto, Japan. 2 Department of Transplant Surgery, Graduate School of Medicine, Nagoya University, Nagoya, Japan. 3 Address correspondence to: Toshimi Kaido, M.D., Ph.D., Division of Hepato-BiliaryPancreatic and Transplant Surgery, Department of Surgery, Graduate School of Medicine, Kyoto University, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto 606-8507, Japan. E-mail: [email protected] T.K. participated in research design, the writing of the paper, the performance of the research, and data analysis. K.O. participated in the performance of the research. Y.F. participated in the performance of the research. T.I. participated in the performance of the research. K.T. participated in research design, the performance of the research, and data analysis. A.M. participated in the performance of the research. Y.O. participated in the performance of the research. S.U. participated in research design and the performance of the research.
Copyright * 2014 by Lippincott Williams & Wilkins ISSN: 0041-1337/14/9708-00 DOI: 10.1097/TP.0000000000000060
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
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Yi NJ, Suh KS, Kim T, et al. Current role of surgery in treatment of early stage hepatocellular carcinoma: resection versus liver transplantation. Oncology 2008; 75(Suppl 1): 124. Poon RT, Fan ST, Lo CM, et al. Long-term survival and pattern of recurrence after resection of small hepatocellular carcinoma in patients with preserved liver function: implications for a strategy of salvage transplantation. Ann Surg 2002; 235: 373. Adam R, Azoulay D, Castaing D, et al. Liver resection as a bridge to transplantation for hepatocellular carcinoma on cirrhosis: a reasonable strategy? Ann Surg 2003; 238: 508. Park MS, Lee KW, Suh SW, et al. Liver Transplantation Versus Liver Resection for the Treatment of Hepatocellular Carcinoma. Liver Transpl 2013; 19(Suppl 1 (6)): S118. Suh KS, Cho EH, Lee HW, et al. Liver transplantation for hepatocellular carcinoma in patients who do not meet the Milan criteria. Dig Dis 2007; 25: 329. Yang SH, Suh KS, Lee HW, et al. A revised scoring system utilizing serum alphafetoprotein levels to expand candidates for living donor transplantation in hepatocellular carcinoma. Surgery 2007; 141: 598. Lee JW, Paeng JC, Kang KW, et al. Prediction of tumor recurrence by 18F-FDG PET in liver transplantation for hepatocellular carcinoma. J Nucl Med 2009; 50: 682. Hong G, Suh KS, Kim HY, et al. Preoperative serum AFP level and serum PIVKA II level and 18F-FDG PET positivity of the tumor predict tumor recurrence better than Milan criteria for patients with HCC in adult-to-adult living donor liver transplantation. Liver Transpl 2012; 18(Suppl 1): S94. Elsharkawi M, Staib L, Henne-Bruns D, et al. Complete remission of postransplant lung metastases from hepatocellular carcinoma under therapy with sirolimus and mycophenolate mofetil. Transplantation 2005; 79: 855. Kornberg A, Kupper B, Tannapfel A, et al. Long-term survival after recurrent hepatocellular carcinoma in liver transplant patients: clinical patterns and outcome variables. Eur J Surg Oncol 2010; 36: 275. Suh KS, Hong G, Kim HY, et al. Outcome of living donor liver transplantation for patients with far advanced hepatocellular carcinoma. Liver Transpl 2012; 18(Suppl 1): S214.
SECTION 6. MANAGEMENT OF EXTENSIVE NONTUMOROUS PORTAL VEIN THROMBOSIS IN ADULT LIVING DONOR LIVER TRANSPLANTATION
Deok-Bog Moon,1 Sung-Gyu Lee,1,2 Chul-Soo Ahn,1 Shin Hwang,1 Ki-Hun Kim,1 Tae-Yong Ha,1 Gi-Won Song,1 Dong-Hwan Jung,1 Gil-Chun Park,1 Jung-Man Namkoong,1 Hyung-Woo Park,1 Yo-Han Park,1 Cheon-Soo Park,1 Kyu-Bo Sung,1 Gi-Young Ko,1 and Dong-Il Gwon1 Background. Patent portal vein (PV) and adequate portal inflow is essential for successful living donor liver transplantation (LDLT). In extensive portal vein thrombosis (PVT) patients, however, complete PV thrombectomy is not feasible particularly at intrapancreatic portion, and subsequently portal flow steal through preexisting sizable collaterals or rethrombosis can occur. To overcome those problems, we introduced interruption of sizable collaterals and intraoperative cine-portogram (IOP), which is useful for diagnosis and treatment of residual PVT and sizable collaterals. Methods. Fourteen percent of adult LDLT (188/1399) had PVT from February 2008 to December 2012 and were subdivided into
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Yerdel’s grades 1, 2, 3, and 4 based on preoperative imaging and operative findings. Considering the severity of PVT and presence of sizable collaterals, the managements were as follows: thrombectomy alone, additional PV plasty, PV stenting, interposition graft, or additional interruption of collaterals. Results. The Yerdel’s grade of PVT patients were 1 (42%), 2 (54%), 3 (3%), and 4 (1%). One hundred one (77%) patients underwent interruption of sizable collaterals. The most common management for PVT was thrombectomy alone in grades 1 and 2, thrombectomy plus PV stenting and/or ballooning in grade 3, and interposition graft in grade 4. In LDLT for PVT patients, 1-year mortality was 9%, and PV-related complication occurred in 5%. The severity of PVT made no difference in the outcome. Conclusion. Multi-disciplinary approaches including surgical correction of PVT, IOP, and interruption of sizable collaterals resulted in excellent outcome, and it was not affected by the severity of PVT. Keywords: Portal vein thrombosis, Adult, Living donor liver transplantation, Management.
eceased donor liver transplantation (DDLT) in patients with portal vein thrombosis (PVT) is no longer considered a contraindication at most centers because of surgical innovations (1Y5). In living donor liver transplantation (LDLT), the management is principally similar to DDLT, but the issue of subjecting a healthy donor to potentially significant morbidity and mortality has led to a critical reassessment of some of the recipient selection criteria that are considered acceptable in DDLT (6). Moreover, based on the greater technical difficulties and the results obtained from DDLT in extensive PVT patients including complete thrombosis of main PV, Yerdel grades 3 and 4 patients, presence of extensive PVT in the recipient has often been considered to be a relative or absolute contraindication in LDLT (7). The scarcity of DDLT in Korea, however, led us to perform ceaseless trials to tackle the extensive PVT in LDLT at our institution and the recent outcomes are not inferior to DDLT for PVT patients. To be a successful LDLT for PVT patient, we have to give a special consideration to the anatomies of both donor’s PV and recipient’s portosplanchnic venous system. In regard to donor PV, it has relatively small diameter corresponding to recipient main PV and short of length compared to deceased whole organ donor. Variant PV anatomy, such as type II or III PV, posterior PV arising from main PV, is also common. There are limited resources of a fresh deceased donor venous conduit for extra-anatomic PV anastomosis. In regard to recipient PV, the diameter of PV
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The authors declare no funding or conflicts of interest. 1 Division of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Korea. 2 Address correspondence to: Sung-Gyu Lee, M.D., F.A.C.S., Division of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, 388-1 Pungnap-dong, Songpa-gu, Seoul 138-736, Korea. E-mail: [email protected] S.-G.L. and D.-B.M. participated in research design. S.-G.L., D.-B.M., C.-S.A. participated in writing of the paper. S.-G.L., D.-B.M., S.H., K.-H.K., T.-Y.H., G.-W.S., D.-H.J., G.-C.P., K.-B.S., G.-Y.K., D.-I.G. participated in performance of the research. J.-M.N., H.-W.P. contributed new reagents or analytic tools. Y.-H.P. and C.-S.P. participated in data analysis.
Copyright * 2014 by Lippincott Williams & Wilkins ISSN: 0041-1337/14/9708-00 DOI: 10.1097/TP.0000000000000060
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is often too small for donor PV because of combined PV stenosis related to chronic organized thrombus, and also sometimes inversely too large after thrombectomy. The quality of recipient PV wall is often poor and paper thin from trauma during dissection and thrombectomy. In case of dual-graft LDLT, right and left PV bifurcations need to be preserved for reconstruction of PVs of both implanting grafts. Complete thrombectomy of extensive PVT during transplantation is often not secured, particularly, at intrapancreatic PV segment, and we should take care of coexistent sizable portosystemic collaterals, which might be the cause of portal flow steal and PV rethrombosis and result in failure of the implanted partial liver graft. To overcome those problems, we introduced interruption of sizable collaterals and intraoperative cine-portogram (IOP) during adult LDLT, which is useful tool for diagnosis and treatment of residual PVT and sizable collaterals. In this article, we described that how to apply our novel approaches for extensive PVT patients and the outcomes of adult LDLT for PVT patients at our institution.
MATERIALS AND METHODS From February 2008 through December 2012, a total of 1679 adult patients underwent liver transplantation (LT) consisting of 1399 cases of LDLT and 280 cases of DDLT at Asan Medical Center, Seoul, Korea. When we exclude the patients who had tumor-related PVT confirmed pathologically, a total number of nontumorous PVT patients were 223 patients (13.3%) consisting of 188 cases (14.4%) of LDLT and 35 cases (12.5%) of DDLT. Both Doppler ultrasound and 3-dimensional computed tomography (3DCT) scans were performed in all patients within 1 month before LT. Based on the degree and extent of PVT-assessed preoperative Doppler ultrasound and 3DCT scan, PVT was classified into four grades (Yerdel grading), that is, grade 1: the PV minimally or partially thrombosed, less than 50% of the vessel lumen; grade 2: more than 50% occlusion of the PV including total occlusion; grade 3: complete thrombosis of both PV and proximal superior mesenteric vein (SMV); and grade 4: complete thrombosis of the PV as well as proximal and distal SMV (5). In addition, we arbitrarily classified PVT patients into two groups in consideration of difficulty in surgical technique and simplicity of comparison, that is, partial PVT: less than 90% occlusion of the PV; complete PVT: 90% to 100% near complete occlusion of the PV. They included 173 male and 50 female patients with a median age of 54 years (range 18 Y 70). The original disease, their Child-Turcotte-Pugh classification, the Model for End-Stage Liver Disease (MELD) score, and preoperative complications are shown in Table 1.
SURGICAL TECHNIQUES PVT can result in development of numerous minute or sizable pericholedochal varix and cumbersome bleeding may occur during dissection of hepatic hilum. In addition, PV thrombectomy is one of the most critical procedures, and time consuming PV plasty is often necessary. As a result, dissection of hepatic hilum is performed as a last procedure after completion of another hepatectomy procedure. When the large collateral veins functioning main splanchnic venous outflow are used for portal inflow vessel in form of end-to-end anastomosis such as left renal vein (LRV) draining large splenorenal shunt (SRS), or when large amount of ascites are present in the absence of large collateral veins, indicating unrelieved severe portal hypertension, venovenous bypass of the splanchnic blood flow through the interposition graft to decompress portal hypertension is useful for avoiding bowel congestion and also reduction of bleeding.
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Most of grade 1 PVT can be managed by low dissection and eversion thrombectomy with end-to-end donor-recipient portal anastomosis. Some of grade 2 and 3 PVT can also be resolved with thrombectomy. However, although portal blood flow look like full restoration, complete thrombectomy, not leaving remnant PVT and/or stenosis, is not feasible in many grades 2 and 3 patients, particularly at intrapancreatic segment of PV. Furthermore, sizable portosystemic collaterals often coexist with residual PVT (Fig. 1). Therefore, we evaluate portal blood flow from the divided PV stump after thrombectomy and also before and after interruption of sizable portosystemic collaterals to decide whether the thrombectomized PV can be adequate portal inflow to the liver graft or not. If recipient’s PV is inadequate for portal inflow, interposition graft is employed from SMVor LRV of patient with large spontaneous splenorenal shunt (SRS). When recipient’s PV was decided to use for portal inflow, measurement of its luminal diameter was performed. If the PV diameter, expected to anastomose to the graft PV, is less than 1 cm after thrombectomy, we perform PV plasty with autologous bisected great saphenous vein (GSV) to enlarge its diameter and avoid anastomotic stricture because PV diameter should be at least 1 cm diameter to relieve PV stenosis and also to effectively decompress portal hypertension by virtue of our experiences. If recipient’s PV has too large and thick wall after thrombectomy in contrast to the graft PV with small and thin wall, we perform funnel-shape fencing to the graft PV with bisected GSV at the back-table for adjustment of graft PV to the recipient’s PV and anastomosis without difficulty (Fig. 2). In addition, surgical interruption of sizable collaterals is held after engraftment and perfusion to give adequate portal flow into the graft. In case of grade 4 PVT, when there is a suitable large splanchnic collateral vein satisfying at least 1 cm size in diameter such as coronary vein, inferior mesenteric vein, LRV in case of splenorenal shunt, SMV branch or pericholedochal vein, it can be used as a portal inflow vessel by interposition graft during adult LDLT. When pericholedochal vein is
TABLE 1. Demographic data of patients with portal vein thrombosis (PVT) Original disease Liver cirrhosis without HCC Liver cirrhosis with HCC Autoimmune hepatitis Idiopathic portal vein thrombosis Portal bilopathy Wilson’s disease Congenital hepatic fibrosis Biliary atresia Preoperative condition Child-Turcoote-Pugh classifications (A/B/C) MELD score Below 15/ 15j25 / above 25 Ascities (no / controlled / uncontrolled) Gastrointestinal bleeding (no / yes) Encephalopathy (no / yes)
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No. 136 80 3 1 1 1 1 1 29 / 78 / 116 21.2T7.6 96 / 90 / 37 20 / 120 / 83 105 / 118 123 / 100
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Chen et al.
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FIGURE 1. A, Preoperative 3-dimensional computed tomography (3D-CT) revealed complete portal vein thrombosis (PVT) and large coronary vein and splenorenal shunt draining into left renal vein, which drained most of splanchnic blood flow in A1 and 2. Intraoperative cine-portogram (IOP) showed no residual PVT after thrombectomy and disappearance of portosystemic collaterals after ligation of coronary vein in A3. B, Preoperative 3D-CT revealed complete PVT extended in proximal superior mesenteric vein and large coronary vein in A1 and 2. IOP after PVT thrombectomy showed residual PVT at the intrapancreatic PV and proximal SMV and portal flow steal through persistent large coronary vein in B3.
present in form of less than 1 cm sized small multiple veins, pericholedochal vein is usually inadequate for portal inflow vessel because of technical difficulties and little possibility of effective routes for portal decompression. In the absence of a suitable collateral vein, there is still no effective solution in adult LDLT, although portocaval hemitransposition has been advocated in DDLT or pediatric LDLT (8, 9). When artificial ringed polytetrafluoroethylene (PTFE) vascular graft was necessary as an interposition graft in the absence of available fresh cadaveric vessel, vascular fence using bisected GSV was intervened between the both ends of ringed PTFE graft and collateral vein and donor PV respectively to avoid disastrous event from the disparities of their diameter and vessel wall conditions, as described by ours (10).
APPLICATION OF IOP We initiated the IOP during LDLT on March 2003 to overcome the limitations of intraoperative Doppler ultrasound that had been used to estimate the adequacy of portal inflow (11, 12). The IOP can be performed not only in LDLT but also in DDLT to precisely visualize the significant spontaneous portosystemic collaterals not detected by intraoperative Doppler ultrasound, and monitor the completeness of collateral ligation. In addition, it can be a useful treatment tool for remained PVT or stenosis and surgically uninterrupted sizable collaterals through PV stenting (Wallstent, Boston Scientific or Zilver stent, Cook) and coil embolization of collaterals respectively. The stent are made of Nitinol shape-memory alloy consisting nikel and titanium. There might be a possibility of re-thrombosis after stenting in terms of long-term follow-up, and all the patients who underwent PV stenting are treated with Coumadin. The
target of prothrombin time (INR) is 1.5Y2.5. However, rethrombosis rarely occur during early period of portal venous stenting if large portosystemic collateral vessels are effectively interrupted and all the splanchnic venous flow goes into the liver graft through PV on IOP. It can be performed through inferior mesenteric vein or superior mesenteric branches under fluoroscope. During IOP, we should obtained two types of portograms including SMV and splenic vein (SV) portogram respectively in order to visualize the whole splanchnic venous system (Fig. 3). After PV thrombectomy for grades 1, 2, and some of 3, we perform IOP to evaluate whether PVT is completely removed or not. Based on IOP, we perform PV stenting or additional ballooning when the luminal diameter is less than 1 cm, or the degree of luminal narrowing is more than 50% of cross-section area despite maintenance of more than 1 cm luminal diameter. When more than 1 cm luminal diameter is maintained at the remained thrombus level without floating thrombus and portal flow steal is absent, additional treatment is usually not necessary. For some of grades 3 and 4 patients with sizable collaterals who needs jump graft for portal vein reconstruction, we sometimes perform IOP after laparotomy to decide the best portal inflow vessel among the several possible splanchnic veins or collaterals and also to decide appropriate interruption site for avoidance of portal flow steal.
RESULTS Among 223 patients with PVT, 211 patients (94.6%) were diagnosed preoperatively. Twelve patients (5.4%) were diagnosed during the transplant procedure, but all the patient belonged grade 1 and additional management except thrombectomy was not necessary. Based on occlusive grade
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FIGURE 2. A, Preoperative 3-dimensional computed tomography (3D-CT) revealed complete portal vein thrombosis (PVT) extended into proximal superior mesenteric vein (SMV) in A1. The portal vein (PV) diameter was measured more than 2 cm in A2, and we performed funnel-shape fencing to the graft PV with bisected great saphenous vein (GSV) such at the back-table as schema of A3 for easy and safe anastomosis with large recipient’s PV. A4 is completion view, and white arrowhead indicate GSV fence intervening between donor PV and recipient’s PV indicated by white arrow. B, Preoperative 3D-CT revealed obliterated PV with chronic organized PVT and large coronary vein in B1. Eversion PV thrombectomy was performed in B2 and PV plasty with bisected GSV was performed to enlarge PV diameter more than 1 cm in B3. B4 is the completion view of PV reconstruction showing no stenosis at the suprapancreatic PV.
of PV, 77% (171/223) had partial PVT, and 23.3% (52/223) had complete PVT. According to Yerdel grade, 93 had grade 1 (42%), 120 grade 2 (54%), 7 grade 3 (3%), and 3 grade 4 (1%). One hundred seventy-one patients (77%) had sizable portosystemic collaterals and needed surgical interruption and/or coil embolization during IOP for maintenance of adequate portal blood flow without portal flow steal.
Table 2 shows the operative management of PVT between partial PVT and complete PVT. In partial PVT, thrombectomy only (54%, 93/171) was the most common surgical procedure. In complete PVT, however, thrombectomy and PV stenting and/or ballooning under IOP (33%, 17/52) was the most common management. PV plasty to correct PV stenosis related to chronic organized PVT was
FIGURE 3. Intraoperative portogram (IOP) was checked after engraftment. Both superior mesenteric vein portogram (A) and splenic vein portogram should be checked to visualize the whole splanchnic venous system.
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TABLE 2. Management of portal vein thrombosis (PVT) during liver transplantation Methods Thrombectomy Thrombectomy and PV plasty Thrombectomy and PV plasty and PV stenting and/or ballooning Thrombectomy and PV stenting and/or ballooning Interposition graft Choledochal varix-portal anastomosis
Partial (n=171)
Complete (n=52)
93 (54%) 17 (10%) 20 (12%)
10 (19%) 3 (6%) 9 (17%)
41 (24%)
17 (33%)
0 0
12# (23%) 1 (2%)
Abbreviations: PV, portal vein. # Portal inflow of the 12 interposition grafts consisted of 6 left renal vein, 3 superior mesenteric vein, 1 inferior mesenteric vein, 1 coronary vein, 1 mesenteric collateral vein.
necessary in 22% (37/171) of partial PVT and 23% (12/52) of complete PVT. The portal inflow vessels used for interposition jump graft were the left renal vein (renoportal anastomosis) (50%, 6/12), SMV (25%, 3/12), inferior mesenteric vein, coronary vein, and mesenteric collaterals in 1 patient, respectively. The operative management according to Yerdel grade as followings. Grade1 consisted of thrombectomy only (67%, 62/93), thrombectomy and PV stenting and/or ballooning (20%, 19/93), thrombectomy and PV plasty (12%, 11/93), and additional PV stenting (1%, 1/93). Grade 2 consisted of thrombectomy only (34%, 41/120), thrombectomy and PV stenting and/or ballooning (28%, 34/120), thrombectomy and PV plasty with stenting (23%, 28/120), and interposition jump graft (7%, 8/120). Grade 3 consisted of thrombectomy and PV plasty with stenting (71%, 5/7) and interposition jump graft (29%, 2/7). Grade 4 consisted of interposition jump graft (67%, 2/3) and choledochal varix-PV anastomosis (33%, 1/3). The overall incidence of PVT related complication is 4.9% (11/223), and it consisted of PV stenosis (45%, 5/11), TABLE 3.
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rethrombosis (18%, 2/11), PV tearing (18%, 2/11), and portal flow steal related graft dysfunction (18%, 2/11). PV stenosis and rethrombosis did not occur in patients who underwent PV stenting but in patients who underwent PV thrombectomy only. PV tearing developed from PV stenting into relatively small PV with paper-thin wall in one patient, and from PV ballooning with inadequately large-diameter balloon in another patient. Although surgical ligation of sizable collaterals was performed at the time of PV thrombectomy and stenting, portal flow steal related graft dysfunction occurred in 2 patients because complete evaluation of whole splanchnic venous system on IOP was not held through both SMV and SV portogram and we missed a chance to interrupt residual sizable collaterals. Hospital mortality occurred in five patients (2%, 5/223), and the primary causes were rethrombosis in 2 patients, portal flow steal related graft dysfunction in 2 patients, and PV tearing in 1 patients (Table 3). One patient underwent retransplantation on postoperative days 53 using deceased donor whole liver due to not PV related complication but hepatic artery injury related delayed hepatic arterial thrombosis. He had grade 4 PVT but sizable pericholedochal varix and mesenteric collateral were present. Left hepatic artery (LHA) was the only available arterial inflow in the hepatic hilum because dissection for other hepatic arteries was not possible from copious bleeding and cavernous transformation of hepatic hilum. Intimal detachment of hepatic arterial wall after hilar dissection developed and mural hematoma propagated into the whole celiac arterial system. The overall 1- and 5-year survival rates in PVT patients after LT were 88% and 84%, respectively. The 1- and 5-year survival rates in LDLT were 91% and 87%, and the difference between PVT and non-PVT patients was negligible when compared to previous report (13). The 1-year and 5-year survival rate in DDLT were 69% and 69% respectively, significantly lower survival rate than LDLT. It was not related to management difference but resulted from the poorer preoperative status among DDLT patients (Fig. 4). The 1- and 5-year survival rate after LDLT for PVT patients was not different between partial and complete PVT. Furthermore, Yerdel grades 3 and 4 patients are all alive without
Portal vein related complications after liver transplantation in patients with PVT
No.
PVT
Type of LT
Management of PVT
Complication
Time of complication
Outcome
1 2 3 4 5 6 7 8 9 10 11
Partial Partial Partial Partial Partial Partial Partial Complete Partial Partial Complete
LDLT LDLT LDLT DDLT LDLT LDLT LDLT LDLT LDLT LDLT LDLT
Incomplete thrombectomy Thrombectomy + PV stent Thrombectomy + PV stent Incomplete thrombectomy Thrombectomy only Thrombectomy only Thrombectomy + PV stent Thrombectomy only Thrombectomy only Thrombectomy + ballooning Thrombectomy only
Rethrombosis PV tearing Portal flow steal through LGV Rethrombosis PV stenosis PV stenosis Portal flow steal through IMV PV stenosis PV stenosis) PV rupture PV stenosis
Day 0 Day 0 Day 53 Day 2 10 months Day 14 Day 6 4 months 3 months Day 0 6 months
Dead Dead Dead Dead Alive Alive Dead Alive Alive Alive Alive
Abbreviations: PVT, portal vein thrombosis; LT, liver transplantation; LDLT, living donor liver transplantation; DDLT, deceased donor liver transplantation; PV, portal vein; LGV, left gonadal vein; IMV, inferior mesenteric vein.
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FIGURE 4. Overall patient survival rates in patients with portal vein thrombosis. A, After liver transplantation. B, Comparison between living donor liver transplantation and deceased donor liver transplantation.
PV-related complication, and there is no difference between grades 1 and 2 PVT patients (Fig. 5).
DISCUSSION Preexisting PVT is no more contraindication in DDLT (1Y5), and LDLT for PVT patients also has been performed in some centers (14Y16). Large proportion among extensive PVT patients including complete PVT, or Yerdel grade 3 and 4, however, are excluded from LDLT or the LDLT should be delayed until a DDLT becomes available for an extraanatomic PV reconstruction (15). The plausible explanation is the possibility of extreme difficulty in hilar dissection due to extensive collateral formation and inflammatory changes around the PV (16). For LDLT, recipient PV should be long enough because the graft PV is very short, and the HA should be preserved up to second-order branches to adjust the size and the length because the graft HA is short and small. Dissection of HA without intimal dissection is one of the key procedure to guarantee successful LDLT. As a result, successful completion of the described procedures is very difficult for patients with extensive PVT. At our
institution, however, when we consider LT for PVT patients, the decision for LDLT or DDLT has not been affected by the severity of PVT but by the presence of available donor except grade 4 diffuse portomesenteric thrombosis patients without sizable collaterals that cavo-portal hemitransposition or multivisceral transplantation is the only possible treatment option in the setting of DDLT. The incidence of PVT among LDLT patients at our institution was 14.4%, similar to the incidence in DDLT patients, which was 12.5%. Restoration and maintenance of the normal portal flow is absolutely essential for good graft function and also regeneration of the partial liver graft after LDLT. Hence, we made it a rule to secure luminal diameter of PV at least 1 cm through the whole length and interruption of sizable portosystemic collaterals. For effective thrombectomy during LDLT, dissection of PV from the right and left portal bifurcation to the splenomesenteric confluence level is necessary. However, it is feasible for only a few patients with extensive PVT because access to the intrapancreatic portion of PV is difficult because of high risk of uncontrollable copious bleeding from the preexisting extensive collaterals. At our institution, effective
FIGURE 5. Overall patient survival rate in patients with portal vein thrombosis (PVT) according the severity. A, Comparison between partial and complete PVT. B, Comparison between Yeldel’s grade 1, 2, 3, and 4 PVT.
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thrombectomy that assure normal portal flow was not possible for 33% of grade 1 PVT, 66% of grade 2 PVT, and all the grade 3 and 4 patients. Furthermore, 77% of PVT patients had large portosystemic collaterals on preoperative 3D-CT scan that needed interruption during LT. As a special measure to tackle those problems, we routinely performed IOP during LT for PVT patients and evaluated the completeness of thrombectomy and presence of residual portosystemic collaterals in the splanchnic venous system and also treated them under IOP. As an additional procedure to normalize portal flow after PV thrombectomy, we performed PV plasty to alleviate PV stenosis related with chronic organized PVT in 45% (49/110) among incompletely thrombectomized grade 1 and 2 PVT patients. However, 59% (29/49) of PV plasty patients needed PV stenting additionally to relieve residual PV stenosis at the intrapancreatic PV segment during IOP. Although PV was not stenotic in 73% (156/213) at the suprapancreatic PV segment after PV thrombectomy among grade 1 and 2 PVT patients, 34% (53/156) had residual PVT at the intrapancreatic PV segment and PV stenting was required to maintain luminal diameter of PV. Two third (8/12) of interposition jump graft patients belonged to grade 2 PVT, and 71% (5/7) of grade 3 PVT patients, on the other hand, could be treated by additional PV stenting and/or balloon dilatation under IOP. All the 3 patients of grade 4 PVT at our institution underwent LDLT using large portosystemic collaterals as a portal inflow vessel to establish the portal flow, and IOP was useful to decide which collateral vessels could be used for portal inflow. The necessity for interposition jump graft was decided preoperatively after review of pre-operative 3D-CT scanned within 1 month. The eighty three percent (10/12) of interposition jump graft was performed with LDLT. In the early period, the LDLTs were performed only when fresh cadaveric vessel graft was prepared because the patency rate of cryopreserved vein graft was not satisfactory due to development of aneurysm, thrombosis, stricture (17, 18). Hence, some of recipient candidates requiring interposition jump graft lost opportunity to undergo LT under scarcity of deceased organ donation. Since we successfully performed renoportal anastomosis with ringed-PTFE interposition graft in January 2010, 12 to 16 mm diametered artificial PTFE vascular grafts have been used in all the 9 patients requiring interposition jump graft on LDLT for timely LT without worsening the patient’s condition any more. All patients received low molecular weight heparin for 7 days and vitamin K antagonists (target INR 1.5Y2.0) have been used permanently to prevent foreign body reaction related delayed thrombosis. Until now, all the artificial interposition grafts are patent without thrombosis. At our institution, the 1-year mortality of PVT patients after LDLT was 9%, and the incidence of PV related complication was only 5% (11/223). To our knowledge, it is one of the best outcomes throughout the field of LDLT and DDLT also. It was resulted from the efforts to establish normal portal flow without portal flow steal through combined approaches including surgical managements such as thrombectomy, PV plasty, interruption of large portosystemic collaterals, and interposition jump graft if necessary, and radiologic evaluation for residual PV stenosis, thrombus, and sizable collaterals, and radiologic intervention such as PV stenting and/or ballooning, and coil embolization
Chen et al.
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under the guidance of IOP. IOP was an extremely useful tool to tackle the PVT patients during LT, but inadequate application of PV stenting and/or ballooning and incomplete evaluation of splanchnic venous system can result in PV tearing and portal flow steal respectively. The incidence of rethrombosis of the PV was 1% (2/223) and occurred in the early period of this study. Both cases also could have been avoided if we employed IOP appropriately. Considering the 5 cases with delayed development of PV stenosis after PV thrombectomy only, possibly due to slowly progressing periportal inflammatory reaction, we had better perform PV stenting selectively to avoid delayed PV stenosis when PV diameter or residual PV thrombosis marginally escape from the conditions requiring intervention. In LDLT for PVT patients, not only PV-related complications but also hepatic artery (HA)Yrelated complications is prone to develop because HA injury can often occur during dissection of hepatic hilum when pericholedochal varix or cavernous transformation of hepatic hilum is present, and alternative available arterial inflow vessels or interposing fresh cadaveric iliac artery that have small branches corresponding to graft HA are usually absent. Particularly in extensive PVT patients including grades 3 and 4, we have to perform meticulous dissection to reduce HA injury such as direct arterial wall injury or intimal dissection from mural hematoma propagation. Yerdel’s grade for PVT has been considered the most adequate classification because it correlates the thrombosis extension with the surgical technique and outcome (5, 19). In our series, management of grade 4 PVT corresponded to the report, but in case of grades 1, 2, and 3 PVT patients, Yerdel’s classification based on the data in the setting of DDLT was less practical because the management was not decided by Yerdel’s grade but by the degree of suprapancreatic PV stenosis, residual thrombosis or stenosis at intrapancreatic PV segment after thrombectomy, and presence of large portosystemic collaterals on IOP. In case of grade 1 and 2 PVT, additional managements such as PV plasty, PV stenting and/or ballooning, interposition jump graft, and collateral interruption were necessary. In case of grade 3 PVT PV thrombectomy and PV stent and/or ballooning was more common treatment than interposition jump graft. The preoperative 3D-CT scan and IOP finding after PV thrombectomy were key factors to decide appropriate management, and the described treatment strategy made no difference in the outcomes regardless of severity of PVT.
CONCLUSION LDLT for nontumorous PVT patients achieved excellent outcome in our series, but there must be a direct relation to the postoperative mortality. Multidisciplinary approaches including surgical correction of PVT, IOP, and interruption of sizable collaterals decreased PVT-related complications and showed almost same results despite difference of severity of PVT. In contrast to DDLT, total portomesenteric thrombosis without sizable collaterals is still unsettled task in the field of LDLT. ACKNOWLEDGMENTS The authors would like to acknowledge the efforts of Bo-Hyun Jeong, Seong-Hwa Kang, and Young-In Yun.
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SECTION 7. A NEW THERAPEUTIC STRATEGY ON PORTAL FLOW MODULATION THAT INCREASES DONOR SAFETY WITH GOOD RECIPIENT OUTCOMES
Toshimi Kaido,1,3 Kohei Ogawa,1 Yasuhiro Fujimoto,1 Takashi Ito,1 Koji Tomiyama,1 Akira Mori,1 Yasuhiro Ogura,2 and Shinji Uemoto1
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& Volume 97, Number 8S, April 27, 2014
Abstract. The goal of this study was to examine whether the lower limit of the graft-to-recipient weight ratio (GRWR) can be safely reduced to make better use of the left lobe graft in adult-to-adult living donor liver transplantation in combination with portal pressure control. Beginning December 2007, the acceptable limit for GRWR was lowered to Q0.7% and by April 2009, it was further lowered to Q0.6%. A portal pressure control program targeting a final portal pressure G15 mm Hg was also introduced. The donor complication rate decreased from 13.8% to 9.3%. The overall survival of recipients with GRWR G0.8% did not differ from recipients with a GRWR Q0.8%. In conclusion, the lower limit of the GRWR can be safely reduced to 0.6% using a left lobe graft in adult-toadult living donor liver transplantation in combination with portal pressure control. Keywords: Liver transplantation, Portal flow modulation, Graftto-recipient weight ratio, Small-for-size graft.
onor safety and favorable outcomes of recipients after liver transplantation (LT) are the most important priorities of living donor liver transplantation (LDLT). We recently established a new therapeutic strategy to satisfy both priorities. The strategy consists of grafting the left lobe first, decreasing the lower limit of the graft-to-recipient weight ratio (GRWR) and controlling portal pressure. The present short essay describes details and the value of our new strategy.
D
GRAFT SELECTION One hundred ninety-two adult (age Q18 years) patients underwent LDLT at Kyoto University Hospital between February 2008 and April 2012. The incidence of all donor complications including donors for pediatric recipients is higher when using right (n=500, 44.2%), compared with left or extended lateral lobe grafts (n=762, 18.8%) (PG0.001) (1). Biliary complications are more frequent after right, than after left or extended lateral lobe grafts (12.2% vs. 4.9%, PG0.001). Thus, left lobe grafts are preferable because of lower complication rates and a larger remnant liver that ensures donor safety. However, the lower limit of GRWR and the risk of small-for-size syndrome are critical problems that need to be overcome when using left lobe grafts. Eight hundred and ten adult recipients underwent LDLT at Kyoto University Hospital between February 1999 and March 2012. We have routinely applied the portal The authors declare no funding or conflicts of interest. 1 Division of Hepato-Biliary-Pancreatic and Transplant Surgery, Department of Surgery, Graduate School of Medicine, Kyoto University, Kyoto, Japan. 2 Department of Transplant Surgery, Graduate School of Medicine, Nagoya University, Nagoya, Japan. 3 Address correspondence to: Toshimi Kaido, M.D., Ph.D., Division of Hepato-BiliaryPancreatic and Transplant Surgery, Department of Surgery, Graduate School of Medicine, Kyoto University, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto 606-8507, Japan. E-mail: [email protected] T.K. participated in research design, the writing of the paper, the performance of the research, and data analysis. K.O. participated in the performance of the research. Y.F. participated in the performance of the research. T.I. participated in the performance of the research. K.T. participated in research design, the performance of the research, and data analysis. A.M. participated in the performance of the research. Y.O. participated in the performance of the research. S.U. participated in research design and the performance of the research.
Copyright * 2014 by Lippincott Williams & Wilkins ISSN: 0041-1337/14/9708-00 DOI: 10.1097/TP.0000000000000060
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