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Intervention Review

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Methods to decrease blood loss during liver resection: a network meta-analysis

  1. Constantinos Simillis1,
  2. Tianjing Li2,
  3. Jessica Vaughan1,
  4. Lorne A Becker3,
  5. Brian R Davidson1,
  6. Kurinchi Selvan Gurusamy1,*

Editorial Group: Cochrane Hepato-Biliary Group

Published Online: 2 APR 2014

Assessed as up-to-date: 16 JUL 2012

DOI: 10.1002/14651858.CD010683.pub2

How to Cite

Simillis C, Li T, Vaughan J, Becker LA, Davidson BR, Gurusamy KS. Methods to decrease blood loss during liver resection: a network meta-analysis. Cochrane Database of Systematic Reviews 2014, Issue 4. Art. No.: CD010683. DOI: 10.1002/14651858.CD010683.pub2.

Author Information

  1. 1

    Royal Free Campus, UCL Medical School, Department of Surgery, London, UK

  2. 2

    Johns Hopkins Bloomberg School of Public Health, Department of Epidemiology, Baltimore, Maryland, USA

  3. 3

    SUNY Upstate Medical University, Department of Family Medicine, Syracuse, New York, USA

*Kurinchi Selvan Gurusamy, Department of Surgery, Royal Free Campus, UCL Medical School, Royal Free Hospital, Rowland Hill Street, London, NW3 2PF, UK.

Publication History

  1. Publication Status: New
  2. Published Online: 2 APR 2014


This is not the most recent version of the article. View current version (31 OCT 2016)


References to studies included in this review

  1. References to studies included in this review
  2. References to studies excluded from this review
  3. Additional references
Belghiti 1999 {published data only}
  • Belghiti J, Noun R, Malafosse R, Jagot P, Sauvanet A, Pierangeli F, et al. Continuous versus intermittent portal triad clamping for liver resection: a controlled study. Annals of Surgery 1999;229(3):369-75.
Capussotti 2003 {published data only}
  • Capussotti L, Nuzzo G, Polastri R, Giuliante F, Muratore A, Giovannini I. Continuous versus intermittent portal triad clamping during hepatectomy in cirrhosis. Results of a prospective, randomized clinical trial. Hepato-gastroenterology 2003;50(52):1073-7.
Capussotti 2006 {published data only}
Doklestic 2011 {published data only}
  • Doklestic K, Karamarkovic A, Stefanovic B, Stefanovic B, Milic N, Gregoric P, et al. The efficacy of three transection techniques of the liver resection: A randomized clinical trial. Hepato-gastroenterology 2011;59(117):1501-6.
Lesurtel 2005 {published data only}
  • Lesurtel M, Selzner M, Petrowsky H, McCormack L, Clavien PA, Bismuth, et al. How should transection of the liver be performed? A prospective randomized study in 100 consecutive patients: Comparing four different transection strategies. Annals of Surgery 2005;242(6):814-23.
Lupo 2007 {published data only}
Park 2012 {published data only}
  • Park JB, Joh JW, Kim SJ, Kwon CH, Min Chun J, Man Kim J, et al. Effect of intermittent hepatic inflow occlusion with the Pringle maneuver during donor hepatectomy in adult living donor liver transplantation with right hemiliver grafts: a prospective, randomized controlled study. Liver Transplantation 2012;18(1):130-8.
Petrowsky 2006 {published data only}
  • Petrowsky H, McCormack L, Trujillo M, Selzner M, Jochum W, Clavien PA. A prospective, randomized, controlled trial comparing intermittent portal triad clamping versus ischemic preconditioning with continuous clamping for major liver resection. Annals of Surgery 2006;244(6):921-8; discussion 8-30.
Smyrniotis 2005 {published data only}
  • Smyrniotis V, Arkadopoulos N, Kostopanagiotou G, Farantos C, Vassiliou J, Contis J, et al. Sharp liver transection versus clamp crushing technique in liver resections: A prospective study. Surgery 2005;137(3):306-11.

References to studies excluded from this review

  1. References to studies included in this review
  2. References to studies excluded from this review
  3. Additional references
Aldrighetti 2006 {published data only}
  • Aldrighetti L, Pulitano C, Arru M, Catena M, Finazzi R, Ferla G. "Technological" approach versus clamp crushing technique for hepatic parenchymal transection: a comparative study. Journal of Gastrointestinal Surgery 2006;10(7):974-9.
Arita 2005 {published data only}
Belghiti 1996 {published data only}
Campagnacci 2007 {published data only}
  • Campagnacci R, De Sanctis A, Baldarelli M, Di Emiddio M, Organetti L, Nisi M, et al. Hepatic resections by means of electrothermal bipolar vessel device (EBVS) LigaSure V: early experience. Surgical Endoscopy 2007;21(12):2280-4.
Capussotti 2012 {published data only}
  • Capussotti L, Ferrero A, Russolillo N, Langella S, Lo Tesoriere R, Vigano L. Routine anterior approach during right hepatectomy: results of a prospective randomised controlled trial. Journal of Gastrointestinal Surgery 2012;16(7):1324-32.
Chapman 2000 {published data only}
  • Chapman WC, Clavien PA, Fung J, Khanna A, Bonham A. Effective control of hepatic bleeding with a novel collagen-based composite combined with autologous plasma: results of a randomized controlled trial. Archives of Surgery 2000;135(10):1200-4; discussion 5.
  • Chapman WC, Wren SM, Lebovic GS, Malawer M, Sherman R, Block JE. Effective management of bleeding during tumor resection with a collagen-based hemostatic agent. American Surgeon 2002;68(9):802-7.
Chapman 2007 {published data only}
  • Chapman WC, Singla N, Genyk Y, McNeil JW, Renkens Jr KL, Reynolds TC, et al. A phase 3, randomized, double-blind comparative study of the efficacy and safety of topical recombinant human thrombin and bovine thrombin in surgical hemostasis. Journal of the American College of Surgeons 2007;205(2):256-65.
Chau 2005 {published data only}
  • Chau GY, Lui WY, King KL, Wu CW. Evaluation of effect of hemihepatic vascular occlusion and the Pringle maneuver during hepatic resection for patients with hepatocellular carcinoma and impaired liver function. World Journal of Surgery 2005;29(11):1374-83.
Chen 2006a {published data only}
  • Chen XP, Zhang ZW, Zhang BX, Chen YF, Huang ZY, Zhang WG, et al. Modified technique of hepatic vascular exclusion: effect on blood loss during complex mesohepatectomy in hepatocellular carcinoma patients with cirrhosis. Langenbeck's Archives of Surgery 2006;391(3):209-15.
Cherqui 1999 {published data only}
  • Cherqui D, Goere D, Brunetti F, Malassagne B, Fagniez PL. Selective use of vascular clamps in major hepatectomy. Chirurgie 1999;124(6):632-9.
Chiappa 2007 {published data only}
  • Chiappa A, Zbar AP, Bertani E, Pace U, Viale G, Pruneri G, et al. The ligasure vessel sealer in liver resection: a pilot study. Hepato-gastroenterology 2007;54(80):2353-7.
Chouker 2004 {published data only}
  • Chouker A, Schachtner T, Schauer R, Dugas M, Lohe F, Martignoni A, et al. Effects of Pringle manoeuvre and ischaemic preconditioning on haemodynamic stability in patients undergoing elective hepatectomy: a randomized trial. British Journal of Anaesthesia 2004;93(2):204-11.
Cresswell 2009 {published data only}
  • Cresswell AB, Welsh FK, John TG, Rees M. Evaluation of intrahepatic, extra-glissonian stapling of the right porta hepatis vs. classical extrahepatic dissection during right hepatectomy. HPB: the Official Journal of the International Hepato Pancreato Biliary Association 2009;11(6):493-8.
Dello 2011 {published data only}
  • Dello S, Reisinger K, De Jong M, Van Dam R, Damink SO, Bemelmans M, et al. Intermittent Pringle manoeuvre is associated with gut injury in patients undergoing liver resection. HPB: the Official Journal of the International Hepato Pancreato Biliary Association 2011;13(Suppl 2):48.
  • Reisinger K, Dello S, Van Dam R, Bemelmans MHA, Damink SO, Poeze M, et al. Intermittent Pringle manoeuvre is associated with gut injury in patients undergoing liver resection. Gastroenterology 2011;140(5 Suppl 1):S395.
El-Kharboutly 2004 {published data only}
  • El-Kharboutly WS, El-Wahab MA. The role of adoption of low central venous pressure in hepatic resection with Pringle manoeuvre in reducing blood loss and improving operative outcome. Egyptian Journal of Anaesthesia 2004;20(4):369-76.
El-Moghazy 2009 {published data only}
  • El-Moghazy WM, Hedaya MS, Kaido T, Egawa H, Uemoto S, Takada Y. Two different methods for donor hepatic transection: Cavitron ultrasonic surgical aspirator with bipolar cautery versus Cavitron ultrasonic surgical aspirator with radiofrequency coagulator - a randomized controlled trial. Liver Transplantation 2009;15(1):102-5.
Esaki 2006 {published data only}
Felekouras 2006 {published data only}
  • Felekouras E, Prassas E, Kontos M, Papaconstantinou I, Pikoulis E, Giannopoulos A, et al. Liver tissue dissection: ultrasonic or RFA energy?. World Journal of Surgery 2006;30(12):2210-6.
Figueras 2003 {published data only}
  • Figueras J, Lopez-Ben S, Llado L, Rafecas A, Torras J, Ramos E, et al. Hilar dissection versus the "glissonean" approach and stapling of the pedicle for major hepatectomies: a prospective, randomized trial. Annals of Surgery 2003;238(1):111-9.
Figueras 2005 {published data only}
  • Figueras J, Llado L, Ruiz D, Ramos E, Busquets J, Rafecas A, et al. Complete versus selective portal triad clamping for minor liver resections - a prospective randomized trial. Annals of Surgery 2005;241(4):582-90.
Figueras 2007 {published data only}
  • Figueras J, Llado L, Miro M, Ramos E, Torras J, Fabregat J, et al. Application of fibrin glue sealant after hepatectomy does not seem justified - results of a randomized study in 300 patients. Annals of Surgery 2007;245(4):536-42.
Fischer 2011 {published data only}
  • Fischer L, Seiler CM, Broelsch CE, de Hemptinne B, Klempnauer J, Mischinger HJ, et al. Hemostatic efficacy of tachosil in liver resection compared with argon beam coagulator treatment: an open, randomized, prospective, multicenter, parallel-group trial. Surgery 2011;149(1):48-55.
Frilling 2005 {published data only}
  • Frilling A, Stavrou GA, Mischinger HJ, de Hemptinne B, Rokkjaer M, Klempnauer J, et al. Effectiveness of a new carrier-bound fibrin sealant versus argon beamer as haemostatic agent during liver resection: a randomised prospective trial. Langenbecks Archives of Surgery 2005;390(2):114-20.
Fu 2010 {published data only}
Fu 2011 {published data only}
  • Fu SY, Lau WY, Li GG, Tang QH, Li AJ, Pan ZY, et al. A prospective randomized controlled trial to compare Pringle maneuver, hemihepatic vascular inflow occlusion, and main portal vein inflow occlusion in partial hepatectomy. American Journal of Surgery 2011;201(1):62-9.
Gugenheim 2011 {published data only}
  • Gugenheim J, Bredt LC, Iannelli A. A randomized controlled trial comparing fibrin glue and PlasmaJet on the raw surface of the liver after hepatic resection. Hepato-gastroenterology 2011;58(107):922-5.
Guo 2010 {published data only}
  • Guo JR, Yu J, Jin XJ, Du JM, Guo W, Yuan XH. Effects of acute normovolemic hemodilution on perioperative coagulation and fibrinolysis in elderly patients undergoing hepatic carcinectomy. Chinese Medical Sciences Journal 2010;25(3):146-50.
Hasegawa 2002 {published data only}
  • Hasegawa K, Takayama T, Orii R, Sano K, Sugawara Y, Imamura H, et al. Effect of hypoventilation on bleeding during hepatic resection - a randomized controlled trial. Archives of Surgery 2002;137(3):311-5.
Hashimoto 2007 {published data only}
  • Hashimoto T, Kokudo N, Orii R, Seyama Y, Sano K, Imamura H, et al. Intraoperative blood salvage during liver resection - a randomized controlled trial. Annals of Surgery 2007;245(5):686-91.
Ikeda 2009 {published data only}
  • Ikeda M, Hasegawa K, Sano K, Imamura H, Beck Y, Sugawara Y, et al. The vessel sealing system (LigaSure) in hepatic resection: a randomized controlled trial. Annals of Surgery 2009;250(2):199-203.
Izzo 2008 {published data only}
  • Izzo F, Di Giacomo R, Falco P, Piccirillo M, Iodice R, Orlando AP, et al. Efficacy of a haemostatic matrix for the management of bleeding in patients undergoing liver resection: Results from 237 cases. Current Medical Research and Opinion 2008;24(4):1011-5.
Johnson 1998 {published data only}
  • Johnson LB, Plotkin JS, Kuo PC. Reduced transfusion requirements during major hepatic resection with use of intraoperative isovolemic hemodilution. American Journal of Surgery 1998;176(6):608-11.
Kato 2008 {published data only}
  • Kato M, Kubota K, Kita J, Shimoda M, Rokkaku K, Sawada T. Effect of infra-hepatic inferior vena cava clamping on bleeding during hepatic dissection: a prospective, randomized, controlled study. World Journal of Surgery 2008;32(6):1082-7.
Kim 2007 {published data only}
  • Kim YI, Hwang YJ, Chun JM, Chun BY. Practical experience of a no abdominal drainage policy in patients undergoing liver resection. Hepato-gastroenterology 2007;54(77):1542-5.
Kim 2008 {published data only}
Kohno 1992 {published data only}
  • Kohno H, Nagasue N, Chang YC, Taniura H, Yamanoi A, Nakamura T. Comparison of topical hemostatic agents in elective hepatic resection: a clinical prospective randomized trial. World Journal of Surgery 1992;16(5):966-9; discussion 970.
Koo 2005 {published data only}
  • Koo BN, Kil HK, Choi JS, Kim JY, Chun DH, Hong YW. Hepatic resection by the cavitron ultrasonic surgical aspirator increases the incidence and severity of venous air embolism. Anesthesia and Analgesia 2005;101(4):966-70.
Lentschener 1997 {published data only}
  • Lentschener C, Benhamou D, Mercier FJ, BoyerNeumann C, Naveau S, Smadja C, et al. Aprotinin reduces blood loss in patients undergoing elective liver resection. Anesthesia and Analgesia 1997;84(4):875-81.
  • Lentschener C, Li H, Franco D, Mercier FJ, Lu H, Soria J, et al. Intraoperatively administered aprotinin and survival after elective liver resection for colorectal cancer metastasis - a preliminary study. Fibrinolysis & Proteolysis 1999;13(1):39-45.
Liang 2009 {published data only}
  • Liang G, Wen T, Yan L, Bo L, Wu G, Yang J, et al. A prospective randomized comparison of continuous hemihepatic with intermittent total hepatic inflow occlusion in hepatectomy for liver tumors. Hepato-gastroenterology 2009;56(91-92):745-50.
Liu 1993 {published data only}
  • Liu M, Lui WY. The use of fibrin adhesive for hemostasis after liver resection. Zhonghua Yi Xue Za Zhi (Taipei) 1993;51(1):19-22.
Lodge 2005 {published data only}
  • Lodge JP, Jonas S, Oussoultzoglou E, Malago M, Jayr C, Cherqui D, et al. Recombinant coagulation factor VIIa in major liver resection: a randomized, placebo-controlled, double-blind clinical trial. Anesthesiology 2005;102(2):269-75.
Man 1997 {published data only}
  • Man K, Fan ST, Ng IO, Lo CM, Liu CL, Wong J. Prospective evaluation of Pringle maneuver in hepatectomy for liver tumors by a randomized study. Annals of Surgery 1997;226(6):704-11; discussion 11-3.
Man 2002 {published data only}
  • Man K, Liang TB, Lo CM, Liu CL, Ng IO, Yu WC, et al. Hepatic stress gene expression and ultrastructural features under intermittent Pringle manoeuvre. Hepatobiliary & Pancreatic Diseases International 2002;1(2):249-57.
Man 2003 {published data only}
Matot 2002 {published data only}
Mirza 2011 {published data only}
  • Mirza D, Millar AJ, Sharif K, Vilca-Melendez H, Rela M, Heaton N. The use of Tachosil in children undergoing liver resection with or without segmental liver transplantation. European Journal of Pediatric Surgery 2011;21(2):111-5.
Nagano 2005 {published data only}
  • Nagano Y, Matsuo K, Kunisaki C, Ike H, Imada T, Tanaka K, et al. Practical usefulness of ultrasonic surgical aspirator with argon beam coagulation for hepatic parenchymal transection. World Journal of Surgery 2005;29(7):899-902.
Noritomi 2005 {published data only}
  • Noritomi T, Yamashita Y, Kodama T, Mikami K, Hashimoto T, Konno T, et al. Application of dye-enhanced laser ablation for liver resection. Production of protein sealant on the cut surface of the liver by enhanced thermal energy of low power diode laser. European Surgical Research 2005;37(3):153-8.
Noun 1996 {published data only}
  • Noun R, Elias D, Balladur P, Bismuth H, Parc R, Lasser P, et al. Fibrin glue effectiveness and tolerance after elective liver resection: a randomized trial. Hepato-gastroenterology 1996;43(7):221-4.
Palibrk 2012 {published data only}
  • Palibrk I, Milicic B, Stojiljkovic L, Manojlovic N, Dugalic V, Bumbasirevic V, et al. Clamp-crushing vs. radiofrequency-assisted liver resection: changes in liver function tests. Hepato-gastroenterology 2012;59(115):800-4.
Pietsch 2010 {published data only}
  • Pietsch UC, Herrmann ML, Uhlmann D, Busch T, Hokema F, Kaisers UX, et al. Blood lactate and pyruvate levels in the perioperative period of liver resection with Pringle maneuver. Clinical Hemorheology and Microcirculation 2010;44(4):269-81.
Rahbari 2009 {published data only}
  • Rahbari NN, Zimmermann JB, Koch M, Bruckner T, Schmidt T, Elbers H, et al. IVC CLAMP: infrahepatic inferior vena cava clamping during hepatectomy - a randomised controlled trial in an interdisciplinary setting. Trials 2009;10:94.
Rahbari 2011 {published data only}
  • Rahbari NN, Elbers H, Koch M, Bruckner T, Vogler P, Striebel F, et al. Clamp-crushing versus stapler hepatectomy for transection of the parenchyma in elective hepatic resection (CRUNSH) - a randomized controlled trial (NCT01049607). BMC Surgery 2011;11:22.
Rau 1995 {published data only}
  • Rau HG, Schardey HM, Buttler E, Reuter C, Cohnert TU, Schildberg FW. A comparison of different techniques for liver resection: blunt dissection, ultrasonic aspirator and jet-cutter. European Journal of Surgical Oncology 1995;21(2):183-7.
Richter 2009 {published data only}
Saiura 2006 {published data only}
  • Saiura A, Yamamoto J, Koga R, Sakamoto Y, Kokudo N, Seki M, et al. Usefulness of LigaSure for liver resection: analysis by randomized clinical trial. American Journal of Surgery 2006;192(1):41-5.
Scatton 2011 {published data only}
Schmidt 2008 {published data only}
  • Schmidt T, Koch M, Antolovic D, Reissfelder C, Schmitz-Winnenthal FH, Rahbari NN, et al. Influence of two different resection techniques (conventional liver resection versus anterior approach) of liver metastases from colorectal cancer on hematogenous tumor cell dissemination - prospective randomized multicenter trial. BMC Surgery 2008;8:6.
Schwartz 2004 {published data only}
Shimada 1994 {published data only}
  • Shimada M, Matsumata T, Shirabe K, Kamakura T, Taketomi A, Sugimachi K. Effect of nafamostat mesilate on coagulation and fibrinolysis in hepatic resection. Journal of the American College of Surgeons 1994;178(5):498-502.
Smyrniotis 2002 {published data only}
  • Smyrniotis VE, Kostopanagiotou GG, Gamaletsos EL, Vassiliou JG, Voros DC, Fotopoulos AC, et al. Total versus selective hepatic vascular exclusion in major liver resections. American Journal of Surgery 2002;183(2):173-8.
Smyrniotis 2003 {published data only}
  • Smyrniotis VE, Kostopanagiotou GG, Contis JC, Farantos CI, Voros DC, Kannas DC, et al. Selective hepatic vascular exclusion versus Pringle maneuver in major liver resections: prospective study. World Journal of Surgery 2003;27(7):765-9.
Sugo 2005 {published data only}
  • Sugo H, Matsumoto K, Kojima K, Fukasawa M, Beppu T. Role of ultrasonically activated scalpel in hepatic resection: a comparison with conventional blunt dissection. Hepato-gastroenterology 2005;52(61):173-5.
Takayama 2001 {published data only}
Taniguchi 1992 {published data only}
Van Den Broek 2011 {published data only}
  • Van Den Broek M, Bloemen J, Dello S, Van De Poll M, Damink SO, Dejong C. Randomized controlled trial analyzing the effect of 15 or 30 minutes intermittent Pringle manoeuvre on hepatocellular damage during liver surgery. Journal of Hepatology 2011;55(2):337-45.
Wang 2006 {published data only}
Wang 2011 {published data only}
  • Wang CC, Yap AQ, Chen CL, Concejero AM, Lin YH. Comparison of major hepatectomy performed under intermittent Pringle maneuver versus continuous Pringle maneuver coupled with in situ hypothermic perfusion. World Journal of Surgery 2011;35(4):842-9.
Wong 2003 {published data only}
  • Wong AY, Irwin MG, Hui TW, Fung SK, Fan ST, Ma ES. Desmopressin does not decrease blood loss and transfusion requirements in patients undergoing hepatectomy. Canadian Journal of Anesthesia 2003;50(1):14-20.
Wu 2002 {published data only}
  • Wu CC, Yeh DC, Ho WM, Yu CL, Cheng SB, Liu TJ, et al. Occlusion of hepatic blood inflow for complex central liver resections in cirrhotic patients: a randomized comparison of hemihepatic and total hepatic occlusion techniques. Archives of Surgery 2002;137(12):1369-76.
Wu 2006 {published data only}
  • Wu CC, Ho WM, Cheng SB, Yeh DC, Wen MC, Liu TJ, et al. Perioperative parenteral tranexamic acid in liver tumor resection: a prospective randomized trial toward a "blood transfusion"-free hepatectomy. Annals of Surgery 2006;243(2):173-80.
Xia 2008 {published data only}
  • Xia F, Wang S, Ma K, Feng X, Su Y, Dong J. The use of saline-linked radiofrequency dissecting sealer for liver transection in patients with cirrhosis. Journal of Surgical Research 2008;149(1):110-4.
Yao 2006 {published data only}
  • Yao XH, Wang B, Xiao ZK, Zhou P, Chen CY, Qing ZH. Acute normovolemic hemodilution combined with controlled hypotension in patients undergoing liver tumorectomy. Nan Fang Yi Ke Da Xue Xue Bao 2006;26(6):828-30.
Yokoo 2012 {published data only}
  • Yokoo H, Kamiyama T, Nakanishi K, Tahara M, Fukumori D, Kamachi H, et al. Effectiveness of using ultrasonically activated scalpel in combination with radiofrequency dissecting sealer or irrigation bipolar for hepatic resection. Hepato-gastroenterology 2012;59(115):831-5.

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