Hepatic Artery Reconstruction with Double- Needle Microsuture in Living-Donor Liver Transplantation

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1 LIVER TRANSPLANTATION 12:46 50, 2006 ORIGINAL ARTICLE Hepatic Artery Reconstruction with Double- Needle Microsuture in Living-Donor Liver Transplantation Mutsumi Okazaki, 1 Hirotaka Asato, 1 Akihiko Takushima, 3 Takashi Nakatsuka, 4 Shunji Sarukawa, 1 Keita Inoue, 1 Kiyonori Harii, 3 Yasuhiko Sugawara, 2 and Masatoshi Makuuchi 2 1 Department of Plastic and Reconstructive Surgery and 2 Artificial Organ and Transplantation Division, Department of Surgery, Graduate School of Medicine, University of Tokyo, Bunkyo-ku, Tokyo, Japan; 3 Department of Plastic and Reconstructive Surgery, Kyorin University, School of Medicine, Mitaka-City, Tokyo, Japan; and 4 Department of Plastic and Reconstructive Surgery, Saitama Medical School, Irumagun, Saitama, Japan In living-donor liver transplantation (LDLT), reconstruction of the hepatic artery is challenging because the recipient artery is located deep in the abdominal cavity and the operating field is limited. Also, the hepatic artery of the graft is short and the recipient artery is occasionally damaged. To overcome these difficulties, we developed a double-needle microsuture technique for artery reconstruction. A total of 161 adult patients received 163 LDLTs using this new technique. The first suture was placed at the most difficult point in the artery to be visualized through the microscope. Each stitch was placed from the inner side of the arterial wall to the outer side. The posterior stitch was tied pulling toward the back. The subsequent sutures were advanced anteriorly on either side adjacent to the previous suture. Hepatic artery thrombosis occurred in 4 patients (2.5%), only 2 (1.2%) of which were associated with arterial reconstruction. Intimal dissection developed in the recipient artery in 2 patients (1.2%). Three (50%) of these 6 complications occurred more than 10 days after LDLT. In conclusion, this suturing technique allows for safe intimal adaptation even when the arterial tunica intima is separated from the tunica media, because all stitches are carried from inside of the vessel to the outside, contributing to more satisfactory results. Liver Transpl 12:46 50, AASLD. Received July 5, 2005; accepted July 5, Hepatic arterial thrombosis (HAT) after liver transplantation is a life-threatening event associated with a high rate of graft loss or death. 1 The incidence of HAT during the first 30 days has been reduced to approximately 5% by recent technical advances. 2 HAT is more common, however, in split or living-donor liver transplantation (LDLT). 3 One of the most important processes in LDLT is hepatic artery reconstruction, which in our institute is performed chiefly by plastic microsurgeons using an operating microscope. Anastomosed hepatic arteries in LDLT are larger (2-4 mm) in diameter than those used in the common free flap transfer (1-2 mm). Hepatic artery reconstruction in LDLT is, however, often challenging because the recipient artery is located deep in the abdominal cavity, the operating field is narrow, and the hepatic artery of the graft is short. In addition, the recipient artery is occasionally damaged by severe atherosclerosis, transarterial chemoembolization, or previous surgery (especially hepatectomy and Kasai s operation). In the conventional method of microvascular anasto- Abbreviations: HAT, hepatic artery thrombosis; LDLT, living-donor liver transplantation. Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan and Grants-in-Aid for Research on HIV/AIDS, a multicenter pilot clinical study to compare the safety and efficacy of a steroid-free immunosuppression protocol with monoclonal anti-il2r antibody in hepatitis C virus-positive living-donor liver transplantation, and Research on Measures for Intractable Diseases from the Ministry of Health, Labor and Welfare of Japan. Address reprint requests to Yasuhiko Sugawara, MD, Artificial Organ and Transplantation Division, Department of Surgery, Graduate School of Medicine, University of Tokyo, Hongo, Bunkyo-ku, Tokyo, , Japan. Telephone: ; FAX: ; yasusuga-tky@umin.ac.jp DOI /lt Published online in Wiley InterScience ( American Association for the Study of Liver Diseases.

2 HA RECONSTRUCTION WITH DOUBLE-NEEDLE SUTURE 47 mosis, the arteries were held with a double clamp with 2 stay sutures, which must be rotated for posterior wall anastomosis. 4 A posterior-wall-first anastomotic technique 5,6 has significant advantages for hepatic artery reconstruction in LDLT. In the technique, microsutures are placed in the back wall of the vessel first, and turning over of the microclamp is eliminated. To make the technique easier, we devised a 9-0 nylon thread (4 cm) with a double needle and adopted it in the posteriorwall-first anastomotic technique and named it the double-needle microsuture technique. We analyzed our experience of hepatic artery reconstruction using this method and discuss its problems from the microsurgeon s point of view. PATIENTS AND METHODS Patients The subjects were 161 adult patients who underwent 163 LDLTs from January 2000 to June 2004 using the double-needle microsuture technique. They were the subjects of the study. There were 83 men and 78 women, ranging in age from yr, with a mean of 48 yr. The indications for LDLT included hepatitis virusrelated cirrhosis in 65, cholestatic liver disease including primary biliary cirrhosis and auto immune hepatitis in 50, fulminant hepatitis in 21, biliary atresia in 7, retransplantation in 2, and others in 18. There were 57 patients with hepatocellular carcinoma, 37 of which had a history of transcatheter arterial chemoembolization before LDLT. Liver graft types included right liver with (n 22) or without (n 68) middle hepatic vein, left liver with (n 51) or without (n 5) middle hepatic vein, and right lateral sector (n 17). The graft type selection criteria and donor hepatectomy procedure were described previously. 7,8 In all the LDLTs, the graft artery was anastomosed end-to-end to the recipient artery. The recipient artery was selected according to its patency, the extent of intimal damage, and caliber consistency with that of the graft artery. Surgical Technique For hepatic artery reconstruction, the operating microscope was placed on the right cranial side of the patient. The microsurgeon was positioned at the right side of the operating field and the assistant microsurgeon at the left and the second assistant at the right cranial side for retraction of the liver. A suction drain was placed at the subphrenic space to continuously remove blood and ascites to clear the operating field. The present technique was indicated when it was difficult to turn over the graft artery. A 9-0 monofilament nylon microsuture with double needles (W10V43-9N; Keisei Medical Industrial, Tokyo, Japan; Fig. 1) was specially devised for this technique. Different from the conventional double-needle microsuture, our suture has a short thread (4 cm), which provides the prompt interrupted sutures. The details of our procedure for Figure 1. The 9-0 monofilament nylon microsuture with double needles. The needle is 3/8 circle, 4 mm in length and 0.1 mm in diameter, and the nylon thread is 4 cm in length. the anastomosis are shown in Figure 2. The recipient and graft arteries were clamped with single microclamps to temporarily halt blood flow (Fig. 2A). The first suture was placed at the most difficult point (usually at the middle of the posterior wall) in the artery to be visualized through the microscope. Each stitch was always placed from the inner side of the arterial wall to the outer side (Fig. 2B). The posterior stitch was tied pulling toward the back (Fig. 2C). The subsequent sutures were advanced anteriorly on either side adjacent to the previous suture (Fig. 2D). The anterior vessel wall was sutured with a regular 9-0 microsuture with a single needle (Fig. 2E). When there was a discrepancy in diameter between the graft and recipient artery, each suture was placed to gradually compensate for the discrepancy. Monitoring Patency After reconstruction, the intrahepatic arterial signals were checked using color Doppler ultrasonography. 9 When the graft had multiple arterial stumps, backbleeding from the nonanastomosed stump was checked after reconstruction was complete. When there was sufficient hepatic arterial blood flow in the nonanastomosed stump, no additional arterial reconstruction was performed. 10 Postoperative anticoagulant therapy was administered as described previously. 3 Color Doppler ultrasonography was performed twice a day for 2 weeks to confirm the patency of the intrahepatic arteries. RESULTS Arteries Anastomosed (Table 1) For the recipient artery, the trunks of the right, left, or middle hepatic artery were used in 89 patients (55%), and the branches of the right hepatic artery or left hepatic artery were used in 73 patients (45%). In 1

3 48 OKAZAKI ET AL. TABLE 1. Artery Anastomosed Recipient No. Graft No. Right 56 Right 90 Paramedian branch 32 Lateral branch 17 of right of right Left 28 Left 48 Lateral branch of 27 Branch of left 7 right Branch of left 14 Middle 1 Middle 5 Gastroduodenal 1 juice leakage after splenectomy. This was treated with open drainage on postoperative day 9. There was no hepatic arterial flow in the graft by Doppler ultrasonography on postoperative day 14, which was suspected to be thrombosed. It spontaneously revascularized, however, after the administration of anticoagulants. 11 Patient 3 had simultaneous arterial and portal vein thrombosis, could not receive retransplantation, and died. Patient 4 received LDLT twice before in another institution and received a third LDLT in our hospital. The hepatic artery of the liver graft was anastomosed to the posterior branch of the right hepatic artery of the previous graft. The postoperative course was uneventful for the first 2 weeks. On postoperative day 17, however, there was an intraperitoneal abscess, probably due to bile leakage, and HAT was discovered. In spite of repeated percutaneous drainage of the abscess and administration of anticoagulants and antibiotics, the graft became necrotic and the patient died. In addition to HAT, subintimal hemorrhage developed in the recipient artery due to the intimal dissection in 2 patients (1.2%; Table 2). Figure 2. Schematics of the microvascular anastomosis. (A) The view of the operating field. The recipient and graft arteries are clamped by single microclamps. (B) The first suture is placed at the posterior wall. (C) The posterior stitch is tied, pulling toward the back for good intima adaptation. (D) The subsequent sutures are placed on either side adjacent to the previous suture. (E) The sutures of the anterior wall can be performed with common single-needle microsutures. patient, the gastroduodenal artery was anastomosed because of severe intimal damage due to arterial embolization in the hepatic arteries. There was 1 graft artery in 142 patients (87%), 2 in 20 (12%), and 3 in 1. In all patients, a single arterial reconstruction was performed. 6 Vascular interposition grafts were not used in the series. Hepatic Artery Thrombosis The incidence of HAT was 2.5% (4/163). HAT was detected 8 hours after anastomosis (patient 1), 14 days (patient 2), 3 days (patient 3), and 17 days (patient 4) postoperatively (Table 2). The graft was salvaged in patient 1 by prompt thrombectomy and reanastomosis. Patient 2 received a left liver graft and had pancreatic DISCUSSION The double-needle microsuture technique does not require that the arteries be turned over, which allows for anastomosis of the arteries in situ. The first stitch can be placed at any point along the posterior wall. The next stitch can be advanced along either side of the previous suture. Turnover of the microclip might lacerate the intima, 12 which might cause intimal dissection. This technique is helpful for arteries in which the tunica intima is separated from the tunica media due to serious atherosclerosis or damage resulting from embolization because all stitches are carried from inside of the vessel to the outside, and intimal adaptation can be performed more safely (Fig. 3). In this technique, the surgeon needs to change the needle holder from one needle to the other. This hazard is overcome with experience. In our institute, hepatic artery reconstruction has been performed chiefly by plastic microsurgeons, who had experienced more than 50 free-flap transfers with microvascular anastomosis. Our double-needle microsuture is employed also for the end-to-side anastomosis between flap artery and external carotid artery in head and neck reconstruction using free flap. 13 In

4 HA RECONSTRUCTION WITH DOUBLE-NEEDLE SUTURE 49 TABLE 2. Cases with Arterial Complication No. Age/ gender Disease Complication Onset Graft Graft artery Recipient artery Complication Course 1 46F AIH HAT 8 hours RLS LBr A5 None Salvaged 2 40M HCV HAT 14 POD L C LHA LHA Pancreatic juice leakage Spontaneous revascularization 3 58F PBC HAT 3 POD RLS LBr LBr Portal vein Not salvaged thrombosis 4 31M PSC HAT 17 POD R RHA PBr Liver abscess Not salvaged 5 59M HCV SIH 2 hours L C LHA LHA None Salvaged 6 39M PBC SIH 12 POD L C LHA RHA None Salvaged Abbreviations: HCV, hepatitis C viral cirrhosis; PBC, primary biliary cirrhosis; PSC, primary sclerosing cholangitis; POD, postoperative day; AIH, autoimmune hepatitis; LSRL, lateral sector of right liver; L C, left liver with caudate lobe; RHA, right hepatic artery; LHA, left hepatic artery; LBr, lateral branch of right hepatic artery; PBr, paramedian branch of right hepatic artery; HAT, hepatic artery thrombosis; SIH, subintimal hemorrhage. Figure 3. Schematics of the technique when the tunica intima was separated from the tunica media. All stitches were carried from inside of the vessel to the outside (left panel), allowing for secure sutures with good intima adaptation (right). most cases in LDLT, the hepatic artery anastomosis was completed in about 30 minutes. In hepatic artery reconstruction in LDLT, the complications tend to occur later than those after common free tissue transfers. In common free tissue transfers, more than 80% of vascular thromboses occur within the first 3 postoperative days. 14,15 Serious impairments of the coagulation system in patients with end-stage liver disease might prevent HAT in the early postoperative days. A hypercoagulable state occurs following LDLT due to acceleration of the coagulation system and delayed recovery of the fibrinolytic system. 16 The risk of HAT might increase as liver function recovers. Early diagnosis of HAT and consequent revascularization will lead to graft salvage. 8 Our results suggest that verification of the patency of the intrahepatic arteries with color Doppler ultrasonography is necessary for at least 3 weeks postoperatively. Intimal dissection of the recipient artery is one complication of artery reconstruction, particularly after LDLT. To minimize the incidence of intimal dissection, careful dissection and preparation of the recipient artery are mandatory, in addition to careful adaptation of the tunica intima during arterial anastomosis. Careful selection of an appropriate recipient artery is key to a successful reconstruction. The use of an artery other than hepatic arteries for the recipient is one strategy, including the right gastroepiploic, 17 left gastric, or gastroduodenal artery. Even slight oozy bleeding at the anastomotic site after removal of the microclamp is not negligible in LDLT because most patients have a seriously impaired coagulation system. When oozy bleeding is noted, spontaneous hemostasis cannot be expected, so additional sutures are indicated for hemostasis. If the bleeding is from the posterior wall, the bleeding point from the anastomosis is difficult to control. It is thus recommended that the sutures be inserted close to each other, especially in the posterior wall. Biphasic movements of the vessels, caused by ventilation and heart movement, are another problem. The movement due to ventilation appears problematic; the upper abdominal organs together with the recipient artery move in accordance with ventilation. Handling of the microforceps or needle holders should be adjusted to the ventilation movements. Respiration can be withheld during suture placement as the need arises. Active movement of the recipient artery is easy to overcome, but the large-amplitude movement caused passively by heart movement is occasionally problematic. Quick insertion and release of the needle into the arterial wall is necessary so that the arterial wall is not injured by the needle. The incidence of HAT in LDLT is 2 to 5%, 13,18 20 which is equivalent with our results (2.5%, 4/163). Of the 4 patients with HAT, only 2 (patients 1 and 3) were assumed to be associated with arterial reconstruction. For a lower morbidity rate, it is necessary to create an adequate operating field, select the appropriate recipient artery, and use suitable microinstruments. We believe that our newly developed double-needle microsuture technique is helpful for easier and safer hepatic artery reconstruction in LDLT.

5 50 OKAZAKI ET AL. REFERENCES 1. Sheiner PA, Varma CV, Guarrera JV, Cooper J, Garatti M, Emre S, et al. Selective revascularization of hepatic artery thromboses after liver transplantation improves patient and graft survival. Transplantation 1997;64: Settmacher U, Stange B, Haase R, Heise M, Steinmuller T, Bechstein WO, et al. Arterial complications after liver transplantation. Transpl Int 2000;13: Sugawara Y, Kaneko J, Akamatsu N, Imamura H, Kokudo N, Makuuchi M. Anticoagulant therapy against hepatic artery thrombosis in living donor liver transplantation. Transplant Proc 2002;34: Furuta S, Ikegami T, Nakazawa Y, Hashikura Y, Matsunami H, Kawasaki S, et al. Hepatic artery reconstruction in living donor liver transplantation from the microsurgeon s point of view. Liver Transpl Surg 1997;3: Harris GD, Finseth F, Buncke HJ. Posterior-wall-first microvascular anastomotic technique. Br J Plast Surg 1981; 34: Yamamoto Y, Sugihara T, Sasaki S, Furukawa H, Furukawa H, Okushiba S, et al. Microsurgical reconstruction of the hepatic and superior mesenteric arteries using a back wall technique. J Reconstr Microsurg 1999;15: Sugawara Y, Makuuchi M. Advances in adult living donor liver transplantation: a review based on reports from the 10th anniversary of the adult-to-adult living donor liver transplantation meeting in Tokyo. Liver Transpl 2004;10: Sakamoto Y, Takayama T, Nakatsuka T, Asato H, Sugawara Y, Sano K, et al. Advantage in using living donors with aberrant hepatic artery for partial liver graft arterialization. Transplantation 2002;74: Kasai H, Makuuchi M, Kawasaki S, Ishizone S, Kitahara S, Matsunami H, et al. Intraoperative color Doppler ultrasonography for partial-liver transplantation from the living donor in pediatric patients. Transplantation 1992;54: Ikegami T, Kawasaki S, Matsunami H, Hashikura Y, Nakazawa Y, Miyagawa S, et al. Should all hepatic arterial branches be reconstructed in living-related liver transplantation? Surgery 1996;119: Sugawara Y, Ohtsuka H, Kaneko J, Imamura H, Makuuchi M. Spontaneous revascularization of arterial thrombosis after living donor liver transplantation. Abdom Imaging 2002;27: Uchiyama H, Hashimoto K, Hiroshige S, Harada N, Soejima Y, Nishizaki T, et al. Hepatic artery reconstruction in living-donor liver transplantation: a review of its techniques and complications. Surgery 2002;131(1 Suppl): S200 S Okazaki M, Asato H, Takushima A, Nakatsuka T, Sarukawa S, Harii K. Availability of end-to-side arterial anastomosis to the external carotid artery in free-flap transfer for head and neck reconstruction. Jpn J Head Neck Cancer 2004;30: Kroll SS, Schusterman MA, Reece GP, Miller MJ, Evans GR, Robb GL, et al. Timing of pedicle thrombosis and flap loss after free-tissue transfer. Plast Reconstr Surg 1996; 98: Salgado CJ, Smith A, Kim S, Higgins J, Behnam A, Herrera HR, et al. Effects of late loss of arterial inflow on free flap survival. J Reconstr Microsurg 2002;18: Hashikura Y, Kawasaki S, Okumura N, Ishikawa S, Matsunami H, Ikegami T, et al. Prevention of hepatic artery thrombosis in pediatric liver transplantation. Transplantation 1995;60: Itabashi Y, Hakamada K, Narumi S, Toyoki Y, Totsuka E, Umehara Y, et al. A case of living-related partial liver transplantation using the right gastroepiploic artery for hepatic artery reconstruction. Hepatogastroenterology 2000;47: Wei WI, Lam LK, Ng RW, Liu CL, Lo CM, Fan ST, et al. Microvascular reconstruction of the hepatic artery in live donor liver transplantation: experience across a decade. Arch Surg 2004;139: Turrion VS, Alvira LG, Jimenez M, Lucena JL, Ardaiz J. Incidence and results of arterial complications in liver transplantation: experience in a series of 400 transplants. Transplant Proc 2002;34: Hatano E, Terajima H, Yabe S, Asonuma K, Egawa H, Kiuchi T, et al. Hepatic artery thrombosis in living related liver transplantation. Transplantation 1997;64:

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