Intraoperative Stent Placement in the Portal Vein During or After Liver Transplantation

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1 LIVER TRANSPLANTATION 13: , 2007 ORIGINAL ARTICLE Intraoperative Stent Placement in the Portal Vein During or After Liver Transplantation Yong-Jae Kim, Gi-Young Ko,* Hyun-Ki Yoon, Ji-Hoon Shin, Heung-Kyu Ko, and Kyu-Bo Sung Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Korea The purpose of this research was to evaluate the intermediate effectiveness of intraoperative portal vein stent placement for portal venous stenosis in liver transplantation. We attempted intraoperative portal vein stent placement in 44 portal venous anastomotic stenoses in 36 patients. All patients underwent stent placement via either the inferior or superior mesenteric vein. A total of 22 patients underwent portal vein stent placement simultaneously with liver transplantation, and 14 patients underwent stent placement 1-25 days (mean 5.93 days) after liver transplantation. Of the 22 patients, there was portal vein occlusion in 3 patients and small portal vein ( 6 mm) in 10 patients ( mm; mean size 3.9 mm). Patient follow-up included clinical and laboratory data collection, Doppler ultrasonography (US), and computed tomography (CT). Intraoperative portal vein stent placement was technically successful in all of our study patients, even in 6 patients with total occlusion of the portal vein. A total of 10 study patients underwent thrombectomy of the portal vein, 1 underwent patient portosystemic shunt ligation, and 7 patients had both procedures simultaneously. Portal venous patency has been maintained for 0-56 months (mean 16 months) in 42 (95%) of the 44 stent placements. In conclusion, intraoperative portal vein stent placement is an effective and long lasting treatment modality for treat portal venous stenosis, especially in patients with portal vein occlusion or small sized portal vein. Liver Transpl 13: , AASLD. Received August 17, 2006; accepted November 15, Portal vein steno-occlusive disease is a relatively rare complication following liver transplantation. 1-4 However, when this disease occurs in the early postoperative period, it has very serious consequences. 1,2 Technical factors, such as redundancy of the portal vein, torsion or tight venous anastomosis, and/or displacement of liver graft after transplantation, contribute to early postoperative portal vein steno-occlusive disease. Although such complications have traditionally been treated by surgical management, percutaneous balloon angioplasty or stent placement has been strongly advocated and has more recently been accepted as the initial treatment of choice. In our opinion, however, the liver graft is usually vulnerable to percutaneous transhepatic procedures in the early posttransplantation period (within approximately 2 weeks after liver transplantation) because the graft is usually not fixed. Thus, to minimize potential liver injury during stent placement in the portal vein we therefore prefer intraoperative stent placement to percutaneous transhepatic stent placement in patients with early posttransplantation portal vein steno-occlusive disease. In addition to the technical factors, poor inflow into the portal venous system resulting from hypoplastic portal vein in children, previous portosystemic shunts, spontaneous large gastrorenal or splenorenal shunt, or complete portal vein thrombosis may produce an involution in the size of the portal vein. Consequently, bridge vein graft interposition or thrombectomy is imperative to improve the portal venous inflow. However, the incidence of portal vein steno-occlusive disease is higher in patients undergoing modification of the standard end-to-end veno-venous anastomosis of the portal vein than in patients undergoing a standard anastomosis. 3 To diminish the risk of posttransplantation portal vein steno-occlusive disease, we also perform intraoperative stent placement in the portal vein following sur- Abbreviations: CT, computed tomography; US, ultrasonography. Address reprint requests to Gi-Young Ko, M.D., Department of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Poongnap-2-Dong, Songpa-Ku, Seoul, , Korea. Telephone: (82-2) ; FAX: (82-2) ; kogy@amc.seoul.kr DOI /lt Published online in Wiley InterScience ( American Association for the Study of Liver Diseases.

2 1146 KIM ET AL. TABLE 1. Denominator of the Number of Total Transplants and the Type of Grafts Living-related liver transplantations Cadaveric liver transplantations Right lobe 461 Whole liver 92 Left lobe 165 Right lobe 6 Dual left lobe 126 Left lobe 2 Left lateral segment 34 Left lateral segment 4 Right and left lobe 21 Right posterior segment and left lobe 4 Total number 811 Total number 104 gical portal vein anastomoses in patients with risk for early posttransplantation portal vein steno-occlusive disease. The purpose of this study is to evaluate the intermediate-term efficacy of intraoperative stent placement to treat early posttransplantation portal vein steno-occlusive disease and to prevent portal vein steno-occlusive disease in patients with a risk for early posttransplantation portal vein steno-occlusive disease. MATERIALS AND METHODS Patient Population Between December 1998 and December 2004, 915 patients underwent liver transplantation in our hospital (Table 1), and 36 patents (27 male and 9 female patients) underwent intraoperative portal vein stent placement for prophylaxis and for treatment of portal venous complications. The patients ranged in age from 8 months to 58 yr (mean age 43 yr) and 3 were pediatric patients. A total of 22 patients underwent the procedure simultaneously with liver transplantation for prophylaxis of portal vein steno-occlusive disease (Group A), and 14 patients underwent the procedure 1-25 days (mean time: 6 days) after liver transplantation for treatment of portal vein steno-occlusive disease (Group B). Demographic data of all patients are shown in Table 2. In group A, reconstruction of the portal vein during transplantation was performed by end-to-end anastomosis (n 19) of the recipient and donor portal vein. However, in 5 patients, modified anastomosis of the portal vein (end-to-end anastomosis at the confluence of the recipient superior mesenteric vein and splenic vein [n 1] and interposition of the venous grafts [n 4] due to alteration of the recipient s portal vein, such as occlusion of the portal vein or alteration of the vessel wall) was performed. Thrombosis in the main portal vein was removed prior to anastomosis of the portal veins. Indications for intraoperative stent placement were: 1) a risk of kinking at the portal vein anastomosis (n 7); 2) small size (less than 6 mm in diameter) of the recipient main portal vein after thrombectomy (n 7); 3) small size of the recipient main portal vein with severe portosystemic shunt (n 5); 4) tight suture (n 2); and 5) idiopathic poor inflow into the left-sided liver graft in a patient with dual left lobe grafts (n 1). In group B, diagnosis of portal vein steno-occlusive TABLE 2. Demographic Data of 36 Patients Mean age yr (8 months to 58 yr) Adults 33 Children 3 Underlying disease HBV-LC 17 HBV-HCC 9 Biliary atresia 4 Fulminant hepatitis 2 Wilson s disease 1 Alcoholic cirrhosis 1 Biliary cirrhosis 1 CCC with HBV-related cirrhosis 1 Total 36 Grafted liver Right lobe 17 Dual left lobes 8 Left lobe 6 Whole liver 3 Left lateral segment 2 Total 36 Abbreviations: HBV, hepatitis B virus; HCC, hepatocellular carcinoma; CCC, cholangiocarcinoma. disease was made by combination of Doppler ultrasonography (US), computed tomography (CT), and conventional angiography. The Doppler US criteria of stenosis in pediatric patients were narrowing of the portal vein 2.5 mm in diameter and an acceleration of flow rate at the poststenotic portal vein more than 3 times than that of the prestenotic portal vein. In adults, the criteria of Doppler sonography for the detection of portion vein stenosis were more than a 50% narrowing of the stenotic segment diameter and more than 3 times accelerated velocity at the poststenotic portal vein compared with the main portal vein. The stenosis diameter percentage was also measured on CT or conventional angiography, and a stenosis of more than 50% was considered a significant stenosis. Intraoperative Stent Placement Written informed consent was obtained from each patient or a legal guardian and our institutional review board approved this study. All procedures were performed under general anesthesia. Stent placement was

3 INTRAOPERATIVE STENT PLACEMENT 1147 Figure 1. Steps of intraoperative portal vein stent placement. A. After puncture of the inferior mesenteric vein, portal venogram was obtained using a 5F cobracatheter. B. A inch angled hydrophilic guide wire was advanced into the stenotic or occluded segment of portal vein. C. Balloon angioplasty was performed using balloon which is the same size as stent. D. Portal vein stent placement was performed with the same diameter or with a 10% larger diameter stent than the diameter of the nonstenotic extrahepatic portal vein. performed following portal vein anastomosis in the group A. Four of the 14 patients in group B underwent stent placement following surgical thrombectomy. The remaining 10 patients underwent stent placement without thrombectomy. The steps of intraoperative portal vein stent placement are demonstrated in Figure 1. Under the laparotomy, the inferior mesenteric vein was isolated and was then punctured with an 18-gauge angiocatheter (Becton Dickinson Korea, Seoul, Korea). Under portable C- arm (OEC 9800; GE, Salt Lake, UT) fluoroscopic guidance, the angiocatheter was exchanged for a 7-F sheath over a inch angled hydrophilic guide wire (Terumo, Tokyo, Japan). Following direct main portal venography through the sheath to evaluate the portal venous inflow, the presence of a portal vein stenosis, a kinking of the portal vein, or the portosystemic shunt, the guide wire and a 5-F cobra catheter (Cook, Bloom-

4 1148 KIM ET AL. ington, IN) were used to advance into the intrahepatic portal vein across the portal vein anastomosis. A bolus of heparin (1,000-5,000 unit) then was administered directly into the portal vein. Stent placement was performed using a Wallstent (Boston Scientific, Galway, Ireland) or a Zilver stent (Cook). The stents were 9-14 mm in diameter and cm in length. Stent size for each patient was chosen on the basis of the measured donor s proximal portal vein diameter. Stents were intentionally oversized approximately 1-2 mm to minimize the risk of migration. Patients who required dual stent placement underwent 2 stent placements simultaneously through the inferior mesenteric vein or through both the inferior mesenteric vein and a branch of the superior mesenteric vein. Balloon angioplasty before or after stent placement was performed in 5 patients using a mm in diameter balloon catheter (Ultra-thin Diamond or Synergy; Boston Scientific, Watertown, MA). Balloon inflations were performed for seconds once or twice. Patients who had normal coagulation function or had portal vein thrombosis on prestenting US or CT, were given both intravenous heparin for 2-5 days in order to produce an international normalized ratio of as well as oral anti-platelets (aspirin 100 mg/day and/or dipyridamole 75 mg/day) for 3-6 months following the procedure. However, patients who had coagulopathy were given oral anti-platelets when their coagulation function had normalized. Following stent placement, direct main portal venography was repeated to evaluate the improvement of portal inflow and change of portosystemic shunt, and the puncture site was then closed using a simple closure with 9-0 or 10-0 nylon. The following parameters were documented retrospectively, i.e., technical success and complications, clinical consequence, and the patency of portal venous inflow. Technical success was defined as stent placement in the intended location with fluent portal inflow following stent placement. Complications were defined as necessity of an increased level of care, an additional unplanned surgical manipulation to preserve portal venous inflow, adverse sequelae, or death. The patency of portal venous inflow was evaluated by means of follow-up Doppler US and CT. Doppler US was routinely performed the day after stent placement, weekly until the patient was discharged from our hospital, and then 1, 6, and 12 months after discharge. CT was routinely performed at a 7-10-day interval until the patient was discharged, and then 1, 3, 6, and 12 months after discharge. The Kaplan-Meier survival curve was used to analyze the cumulative patency rate of the stent-inserted portal vein. The unpaired t-test was applied to determine which change of aspartate aminotransferase and alanine aminotransaminase level after stent placement was statistically significant. Analysis was conducted using SPSS software (version 12.0; SPSS, Chicago, IL) with P values lower than 0.05 considered to be significant. RESULTS In total, 44 stents were placed in 36 patents. Eight patients underwent 2 stent placements in the portal vein (in 2 patients in each portal vein of dual grafts, in 5 patients in anterior and posterior portal veins of right lobe graft, and in 1 patient in anastomosis with the saphenous vein graft). No procedural complications occurred. Portal vein stent placement was technically successful in all except 1 stent (43 of 44 patients; 97.7%). In 1 patient who showed 50% stenosis at the anastomosis with sluggish portal inflow into a left lobe graft during dual right and left lobe transplantation, the portal inflow did not improve following successful stent placement in the main portal vein. Follow-up Doppler US and CT demonstrated persistent slow portal inflow and multiple low attenuating foci in the left lobe graft. However, this patient uneventfully recovered his liver function. All patients except 1 infant were discharged 9-93 days (37 20 days) after liver transplantation and stent placement with improved liver function. A 10-monthold girl died of acute rejection 13 days after liver transplantation. This infant had received intraoperative stent placement the day after left lateral segment transplantation due to an occluded main portal vein. Eight days after stent placement, however, as the stent showed acute angulation, a second balloon expandable stent was placed across the initial stent intraoperatively (Fig. 2). Portal inflow improved following the second stent placement; however, the patient died of acute rejection. Thus, the clinical success rate was 97% (35 of 36 patients). Changes of laboratory data before and 2 weeks after stent placement except for this infant, are demonstrated in Table 3. During the mean imaging follow-up period of days (range 97-1,662 days), 2 patients died of recurrent hepatocellular carcinoma 77 and 233 days after stent placement, respectively, and 2 other patients died of intracerebral hemorrhage and an unknown cause 320 and 53 days after stent placement, respectively. However, the last follow-up Doppler US or CT showed patent portal venous flow in those patients. Portal venous abnormality occurred in 2 patients (5.7%) during the follow-up period. A 53-yr-old man who had undergone dual left lobes transplantation and single portal vein stent placement into the left-sided graft revealed stent thrombosis 481 days after transplantation (Fig. 3). Aspiration thrombectomy of the occluded portal vein and a second stent placement were attempted through a percutaneous transhepatic approach in this patient, but traverse through the stent into the main portal vein failed due to severe angulation at the stent margin. Although the left-sided portal vein was not recanalized, he did not have any symptoms of portal hypertension and his liver function was normalized without other treatment until this manuscript was completed (300 days after the diagnosis of portal vein thrombosis). In the other patient with rapidly deteriorated liver function, posttransplantation 203-day fol-

5 INTRAOPERATIVE STENT PLACEMENT 1149 Figure 2. A 10-month-old girl with main portal vein thrombosis 8 days after intraoperative portal vein stent placement. A. The collapse of portal vein stent (arrows) due to acute angulation was noted. B. On portal venogram, the large thrombus (arrows) is seen in the collapsed portion of portal vein stent. C. After balloon expandable stent placement in size of 10 mm diameter, final portal venogram showed patent portal flow. TABLE 3. Laboratory Data Before and 2 Weeks After Stent Placement Group A (n 22) Group B (n 13) Before stent placement 2 weeks after stent placement Before stent placement 2 weeks after stent placement AST (IU/L) (P ) (P ) ALT (IU/L) (P ) (P ) T-Bil (mg/dl) (P ) (P ) Abbreviations: AST, aspartate aminotransferase; ALT, alanine aminotransferase; T-Bil, total bilirubin.

6 1150 KIM ET AL. Figure 3. A 53-year-old man who underwent intraoperative portal vein stent placement in a left-side graft but who did not undergo ligation of portosystemic shunt during liver transplantation. A. Patent portal vein flow (arrows) was noted in the distal portal of stent, and spontaneous gastrorenal shunt (arrowheads) was also noted after 287 days stent placement. B. Obliteration of portal vein (arrows) and more prominent spontaneous gastrorenal shunt (arrowsheads) was noted 481 days after stent placement. low-up CT and Doppler US revealed sluggish portal inflow with several hypertrophied portosystemic collateral veins. Direct main portal venography during surgical ligation of the collateral veins, however, revealed patent portal venous inflow without thrombosis. The patient died of intracerebral hemorrhage 320 days after stent placement. Primary 1- and 2-yr cumulative patency rates after stent placement were % and %, respectively. DISCUSSION Portal vein complications after liver transplantation including anastomotic stenosis and thrombosis are rare, occurring in 1 to 2% of adult orthotopic liver transplantation 1,5,6 and in 3 to 19% of pediatric or living donor liver transplantation. 3,7-12 Portal vein thrombosis after liver transplantation is an uncommon complication; however, the risk increases significantly if the portal vein has been thrombectomized, 13,14 if there is a spontaneous portosystemic shunt with inverted portal flow, 15 if the patient is a child weighing less than 10 kg, or if the cold ischemia time during transplantation has been long. 6 Treatments of portal vein stenosis or thrombosis after liver transplantation were: medical therapy, surgical treatment, percutaneous transluminal angioplasty, and stent placement. Medical therapies were anticoagulant therapy and sclerotherapy. 1,3,16,17 Surgical treatments were thrombectomy and reconstruction, mesocaval shunt, splenorenal shunt, excision of fibrous tissue and donor lymph nodes around the portal vein anastomosis, and retransplantation. 1,4-6,18 Although surgical reconstruction of the anastomosis may be definitive, such intervention can be extremely difficult technically. 1,18 In the present state of things, treatment of portal vein complication after liver transplantation has replaced surgical treatment by percutaneous transluminal angioplasty and stent placement. 3,4,19,20 Route of treatment of the portal vein stenosis or thrombosis is included transhepatic, 3,4,9,19,20 transjugular, transsplenic, 24 and intraoperative inferior mesenteric vein approach. 19,25,26 Bleeding tendency or massive ascites is considered a relative contraindication to the transhepatic or transsplenic approach. Although the transjugular approach is suitable to conditions of bleeding tendency or massive ascites, it is a difficult procedure when there is portal vein thrombosis. Moreover, transplanted liver in the early postoperative period (within 4 weeks) is vulnerable to needle injury in the transhepatic or transjugular approach, and a guide wire could not be negotiated beyond the occluded portal vein by the transhepatic approach. 3,4,9,20,24 But the intraoperative portal vein approach via the inferior mesenteric vein is less injurious to the transplanted liver and is possible for treatment of pediatric patients with ease. Negotiation of the guide wire beyond the occluded segment is feasible in the intraoperative approach. We performed an intraoperative portal vein stent in 14 patients for portal vein thrombosis or stenosis after liver transplantation without any complications and failures. Portal vein thrombosis in the course of end-stage liver disease occurs in 5 to 21% of the cases. 27,28 Lerut et al. 1 analyzed the number, nature of treatment, and outcome of portal vein abnormalities. There were 51 (15.3%) of 393 patients who had surgically significant preexisting portal vein abnormalities. These are thrombosis, hypoplasia, phlebosclerosis, and absent portal vein. The most frequent and most serious condition was portal vein thrombosis. In many cases, liver transplantation can be performed successfully despite portal vein thrombosis, but usually longer and technically more difficult operations are needed in these cases. 1,16,23,29

7 INTRAOPERATIVE STENT PLACEMENT 1151 The technical adjustments required by portal vein abnormalities included thromboendovenectomy, venous graft from the superior mesenteric vein, and cavoportal hemitransposition. 1,28,29 Transjugular intrahepatic portosystemic shunt before liver transplantation is another technical adjustment in patients of portal vein thrombosis. 23 The predisposing factors of portal vein thrombosis after liver transplantation were previous portosystemic shunt, preexisting portal vein thrombosis, prior splenectomy, donor-recipient portal vein diameter mismatch, and limited length of the donor portal vein. 1,30 The intraoperative portal vein stent placement during liver transplantation is a good substitute for surgical adjustment in patients with portal vein abnormalities. In our hospital, if the surgeon judged the portal flow to be poor (e.g., risk of kinking at the portal vein anastomosis, small-sized portal vein, severe portosystemic shunt, or tight suture), direct portogram was performed. Stent placement was based on operation and direct portogram findings. We performed intraoperative portal vein stent placement for prevention of portal vein thrombosis. The main indications of intraoperative portal vein stent placement during liver transplantation in our study were small portal vein size (n 14) and risk of kinking after anastomosis (n 7). Portal vein stent for portal vein stenosis is effective and has good long-term patency. 3,4,12,19,20,24 In Funaki et al., 20 metallic portal vein stents were placed in 12 patients for failure of balloon dilation and recurrence portal vein stenosis, with good patency being maintained for 5-61 months. In our study, the patency rate of the portal vein stent was 95%. There were 2 portal vein thromboses after portal vein stent placement. One of 2 patients had severe coronary varix and gastrorenal shunt. Decreased portal flow due to severe portosystemic shunt may contribute to recurrent portal vein thrombosis. Intraoperative portal vein stent with simultaneous ligation of portosystemic shunt may be more effective for patency of the portal vein stent. In conclusion, intraoperative portal vein stent placement is an effective and long-lasting treatment modality to treat portal venous stenosis, especially in patients with total occlusion or small size of portal vein and may be a substitute for surgical reconstruction of the portal vein in liver transplantation with portal vein thrombosis. REFERENCES 1. Lerut J, Tzakis AG, Bron K, Gordon RD, Iwatsuki S, Esquivel CO, et al. Complications of venous reconstruction in human orthotopic liver transplantation. Ann Surg 1987; 205: Wozney P, Zajko AB, Bron KM, Point S, Starzl TE. 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