World Journal of Surgery

, Volume 29, Issue 11, pp 1384–1396 | Cite as

Vascular Control during Hepatectomy: Review of Methods and Results

  • Vassilios Smyrniotis
  • Charalampos Farantos
  • Georgia Kostopanagiotou
  • Nikolaos Arkadopoulos
Article

Abstract

The various techniques of hepatic vascular control are presented, focusing on the indications and drawbacks of each. Retrospective and prospective clinical studies highlight aspects of the pathophysiology, indications, and morbidity of the various techniques of hepatic vascular control. Newer perspectives on the field emerge from the introduction of ischemic preconditioning and laparoscopic hepatectomy. A literature review based on computer searches in Index Medicus and PubMed focuses mainly on prospective studies comparing techniques and large retrospective ones. All methods of hepatic vascular control can be applied with minimal mortality by experienced surgeons and are effective for controlling bleeding. The Pringle maneuver is the oldest and simplest of these methods and is still favored by many surgeons. Intermittent application of the Pringle maneuver and hemihepatic occlusion or inflow occlusion with extraparenchymal control of major hepatic veins is particularly indicated for patients with abnormal parenchyma. Total hepatic vascular exclusion is associated with considerable morbidity and hemodynamic intolerance in 10% to 20% of patients. It is absolutely indicated only when extensive reconstruction of the inferior vena cava (IVC) is warranted. Major hepatic veins/ and limited IVC reconstruction has been also achieved under inflow occlusion with extraparenchymal control of major hepatic veins or even using the intermittent Pringle maneuver. Ischemic preconditioning is strongly recommended for patients younger than 60 years and those with steatotic livers. Each hepatic vascular control technique has its place in liver surgery, depending on tumor location, underlying liver disease, patient cardiovascular status, and, most important, the experience of the surgical and anesthesia team.

References

  1. 1.
    Sitzmann JV, Greene PS. Perioperative predictors of morbidity following hepatic resection for neoplasm: a multivariate analysis of a single surgeon experience with 105 patients. Ann Surg 1994;219:13–17PubMedGoogle Scholar
  2. 2.
    Shimada M, Matsumata T, Akazawa K, et al. Estimation of risk of major complications after hepatic resections. Am J Surg 1994;167:399–403CrossRefPubMedGoogle Scholar
  3. 3.
    Kooby DA, Stockman J, Ben-Porat L, et al. Influence of transfusions on perioperative and long-term outcome in patients following hepatic resection for colorectal metastases. Ann Surg 2003;237:860–870PubMedGoogle Scholar
  4. 4.
    Takenaka K, Kawahara N, Yamamoto K, et al. Results of 280 liver resections for hepatocellular carcinoma. Arch Surg 1996;131:71–76PubMedGoogle Scholar
  5. 5.
    Delva E, Camus Y, Nordlinger B, et al. Vascular occlusions for liver resections: operative management and tolerance to hepatic ischemia: 142 cases. Ann Surg 1989;209:211–218PubMedGoogle Scholar
  6. 6.
    Wu CC, Kang SM, Ho WM, et al. Prediction and limitation of hepatic tumor resection without blood transfusion in cirrhotic patients. Arch Surg 1998;133:1007–1010PubMedGoogle Scholar
  7. 7.
    Gozzetti G, Mazzioti A, Grazi GL, et al. Liver resection without blood transfusion. Br J Surg 1995;82:1105–1110PubMedGoogle Scholar
  8. 8.
    Takenaka K, Kanematsu T, Fukuzawa K, et al. Can hepatic failure after surgery for hepatocellular carcinoma in cirrhotic patients be prevented? World J Surg 1990;14:123127CrossRefPubMedGoogle Scholar
  9. 9.
    Yamamoto J, Kosuge T, Takayama T, et al. Perioperative blood transfusion promotes recurrence of hepatocellular carcinoma after hepatectomy. Surgery 1994;115:303–309PubMedGoogle Scholar
  10. 10.
    Poon RTP, Fan ST, Ng IOL, et al. Significance of resection margin in hepatectomy for hepatocellular carcinoma: a critical reappraisal. Ann Surg 2000;231:544–551CrossRefPubMedGoogle Scholar
  11. 11.
    Rosen CB, Nagorney DM, Taswell HF, et al. Preoperative blood transfusion and determinants of survival after liver resection for metastatic colorectal carcinoma. Ann Surg 1992;216:493–505PubMedGoogle Scholar
  12. 12.
    Obayashi T, Taniguchi H, Mugitani T, et al. Safety and utility of autologous blood transfusion for resection of metastatic liver tumor. Hepatogastroenterology 2001;48:812–817PubMedGoogle Scholar
  13. 13.
    Arnoletti JP, Brodsky J. Reduction of transfusion requirements during major hepatic resections for metastatic disease. Surgery 1999;125:166–171PubMedGoogle Scholar
  14. 14.
    Melendez JA, Arslan V, Fischer ME, et al. Perioperative outcomes of major hepatic resections under low central venous pressure anaesthesia: blood loss, blood transfusion, and the risk of preoperative renal dysfunction. J Am Coll Surg 1998;187:620–625CrossRefPubMedGoogle Scholar
  15. 15.
    Malassagne B, Cherqui D, Alon R, et al. Safety of vascular clamping for major hepatectomies. J Am Coll Surg 1998;187:482–486CrossRefPubMedGoogle Scholar
  16. 16.
    Descottes B, Thognon P, Valleix D, et al. Major liver resections without vascular clamping: retrospective study of 84 cases. Hepatogastroenterology 1998;45:364–367PubMedGoogle Scholar
  17. 17.
    Cherqui D, Malassagne B, Colau PI, et al. Hepatic vascular exclusion with preservation of the caval flow for liver resections. Ann Surg 1999;230:24–30CrossRefPubMedGoogle Scholar
  18. 18.
    Smyrniotis VE, Kostopanagiotou GG, Kontis JC, et al. Selective hepatic vascular exclusion (SHVE) versus Pringle maneuver in major liver resections; a prospective study. World J Surg 2003;27:765–769PubMedGoogle Scholar
  19. 19.
    Clavien PA, Selzner M, Rüdiger HA, et al. A prospective study in 100 consecutive patients undergoing major liver resection with versus without ischemic preconditioning. Ann Surg 2003;238:843–852PubMedGoogle Scholar
  20. 20.
    Torzilli G, Makuuchi M, Inoue K, et al. No-mortality liver resection for hepatocellular carcinoma in cirrhotic and noncirrhotic patients: is there a way? A prospective analysis of our approach. Arch Surg 1999;134:984–992PubMedGoogle Scholar
  21. 21.
    Torzilli G, Makuuchi M, Midorikawa Y, et al. Liver resection without total vascular exclusion: hazardous or beneficial? An analysis of our experience. Ann Surg 2001;233:167–175CrossRefPubMedGoogle Scholar
  22. 22.
    Takayama T, Makuuchi M, Inoue K, et al. Selective and unselective clamping in cirrhotic liver. Hepatogastroenterology 1998;45:376–380PubMedGoogle Scholar
  23. 23.
    Midorikawa Y, Kubota K, Takayama T, et al. A comparative study of postoperative complications after hepatectomy in patients with and without chronic liver disease. Surgery 1999;126:484–491PubMedGoogle Scholar
  24. 24.
    Lai ECS, Fan ST, Lo CM, et al. Anterior approach for difficult major right hepatectomy. World J Surg 1996;20:314–318CrossRefPubMedGoogle Scholar
  25. 25.
    Stasberg SM, Drebin JA. Linehan D. Use of a bipolar vessel-sealing device for parenchymal transection during liver surgery. J. Gastrointest. Surg. 2002;6:569–574Google Scholar
  26. 26.
    Yamamoto Y, Ikai I, Kume M, et al. New simple technique for hepatic parenchymal resection using a Cavitron Ultrasonic Surgical Aspirator® and bipolar cautery equipped with a channel for water dripping. World J Surg 1999;23:1032–1037PubMedGoogle Scholar
  27. 27.
    Weber JC, Navarra G, Jiao LR, et al. New technique for liver resection using heat coagulative necrosis. Ann Surg 2002;236:560–563CrossRefPubMedGoogle Scholar
  28. 28.
    Staren ED, Gambla M, Deziel DJ, et al. Intraoperative ultrasound in the management of liver neoplasms. Am Surg 1997;63:591–597PubMedGoogle Scholar
  29. 29.
    Luck AJ, Maddern GJ. Intraoperative abdominal ultrasonography. Br J Surg 1999;86:5–16CrossRefPubMedGoogle Scholar
  30. 30.
    Jones RMcL, Moulton CE, Hardy KJ. Central venous pressure and its effect on blood loss during liver resection. Br J Surg 1998;85:1058–1060PubMedGoogle Scholar
  31. 31.
    Wu CC, Yeh DC, Ho WM, 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. Arch Surg 2002;137:1369–1376PubMedGoogle Scholar
  32. 32.
    Cunningham JD, Fong Y, Shriver C, et al. Our hundred consecutive hepatic resections: blood loss, transfusion and operative technique. Arch Surg 1994;129:1050–1056PubMedGoogle Scholar
  33. 33.
    Smyrniotis VE, Kostopanagiotou GG, Gamaletsos EL, et al. Total versus selective hepatic vascular exclusion in major liver resections. Am J Surg 2002;183:173–178PubMedGoogle Scholar
  34. 34.
    Abdalla EK, Noun R, Belgihiti J. Hepatic vascular occlusion: which technique? Surg. Clin. North Am. 2004;84:563–585CrossRefPubMedGoogle Scholar
  35. 35.
    Man K, Fan St, Ng IOL, et al. Prospective evaluation of Pringle maneuver in hepatectomy for liver tumors by a randomized study. Ann Surg 1997;226:704–713CrossRefPubMedGoogle Scholar
  36. 36.
    Elias F, Desruennes E, Lasser P. Prolonged intermittent clamping of the portal triad during hepatectomy. Br J Surg 1991;78:42–44PubMedGoogle Scholar
  37. 37.
    Man K, Lo CM, Liu CL, et al. Effects of the intermittent Pringle maneuver on hepatic gene expression and ultrastructure in a randomized clinical study. Br J Surg 2003;90:183–189CrossRefPubMedGoogle Scholar
  38. 38.
    Belghiti J, Noun R, Malafosse R, et al. Continuous versus intermittent portal triad clamping for liver resection: a controlled study. Ann Surg 1999;229:369–375CrossRefPubMedGoogle Scholar
  39. 39.
    Berney T, Mentha G, Morel PH. Total vascular exclusion of the liver for the resection of lesions in contract with the vena cava or the hepatic veins. Br J Surg 1998;85:485–488PubMedGoogle Scholar
  40. 40.
    Belghiti J, Noun R, Zante E, et al. Portal triad clamping or hepatic vascular exclusion for major liver resection: a controlled study. Ann Surg 1996;224:155161CrossRefPubMedGoogle Scholar
  41. 41.
    Huguet C, Gavelli A, Addario Chieco A, et al. Liver ischemia for hepatic resection: where is the limit? Surgery 1992;111:251–259PubMedGoogle Scholar
  42. 42.
    Hannoun L, Borie D, Delva E, et al. Liver resection with normothermic ischaemia exceeding 1 h. Br J Surg 1993;80:1161–1165PubMedGoogle Scholar
  43. 43.
    Serracino-Inglott F, Habib NA, Mathie RT. Hepatic ischemia-reperfusion injury: review. Am J Surg 2001;181:159–166CrossRefGoogle Scholar
  44. 44.
    Pringle JH. Notes on the arrest of hepatic haemorrhage due to trauma. Ann Surg 1909;48:541–549Google Scholar
  45. 45.
    Belghiti J. Vascular isolation techniques in liver resection. In Blumgart LM, editor, Surgery of the Liver and Biliary Tract, New York, Churchill Livingstone, 2001;1715–1724Google Scholar
  46. 46.
    Detroz B, Honoré P, Denoiseux C, et al. Biology, physiology and physiopathology of clamping during liver surgery. Hepatogastroenterology 1998;45:357–363PubMedGoogle Scholar
  47. 47.
    Decailliot F, Cherqui D, Leroux B, et al. Effects of portal triad clamping on haemodynamic conditions during laparoscopic liver resection. Br J Anaesth 2001;87:493–496CrossRefPubMedGoogle Scholar
  48. 48.
    Delva E, Barberousse JP, Nordlinger B, et al. Hemodynamic and biochemical monitoring during major liver resection with use of hepatic vascular exclusion. Surgery 1984;95:309–318PubMedGoogle Scholar
  49. 49.
    Bismuth H, Castaing D, Garden OJ. Major hepatic resection under total vascular exclusion. Ann Surg 1989;210:13–19PubMedGoogle Scholar
  50. 50.
    Hatano Y, Murakawa M, Segawa H, et al. Venous air embolism during hepatic resection. Anesthesiology 1990;73:1282–1285PubMedGoogle Scholar
  51. 51.
    Smyrniotis V, Kostopanagiotou G, Lolis E, et al. Effects of hepatoprotective backflow on ischemic-reperfusion injuries in liver resections with the Pringle maneuver. J Am Coll Surg 2003;197:949–954CrossRefPubMedGoogle Scholar
  52. 52.
    Cigot JF, Glineur D, Santiago Azagra J, et al. Laparoscopic liver resection for malignant liver tumors: preliminary results of a multicenter European study. Ann Surg 2002;236:90–97Google Scholar
  53. 53.
    Yoshizumi T, Yanaga K, Soejima Y, et al. Amelioration of liver injury by ischemic precontioning. Br J Surg 1998;85:1636–1640CrossRefPubMedGoogle Scholar
  54. 54.
    Howell JG, Zibari GB, Brown MF, et al. Both ischemic and pharmacological preconditioning decrease hepatic leukocyte/endothelial cell interactions. Transplantation 2000;69:300–314PubMedGoogle Scholar
  55. 55.
    Peralta C, Hotter G, Glosa D, et al. Protective effect of preconditioning on the injury associated to hepatic ischemia-reperfusion in the rat: role of nitric oxide and adenosine. Hepatology 1997;25:934–937CrossRefPubMedGoogle Scholar
  56. 56.
    Arai M, Thurman RG, Lemasters JJ. Contribution of adenosine A2-receptors and cyclic adenosine monophosphate to protective ischemic preconditioning of sinusoidal endothelial cells against storage/reperfusion injury in rat livers. Hepatology 2000;32:297–302CrossRefPubMedGoogle Scholar
  57. 57.
    Peralta C, Fernández L, Panés J, et al. Preconditioning protects against systemic disorders associated with hepatic ischemia-reperfusion through blockage of tumor necrosis factor-induced P-selectin up-regulation in the rat. Hepatology 2001;33:100–113CrossRefPubMedGoogle Scholar
  58. 58.
    Fung JJ. Ischemic preconditioning: application in clinical liver transplantation. Liver Transpl. 2001;7:300–301CrossRefPubMedGoogle Scholar
  59. 59.
    Imamura H, Takayama T, Sugawara Y, et al. Pringle’s maneuver in living donors. Lancet 2002;360:2049–2050CrossRefPubMedGoogle Scholar
  60. 60.
    Man K, Fan ST, Ng IOL, et al. Tolerance of the liver to intermittent Pringle maneuver in hepatectomy for liver tumors. Arch Surg 1999;134:533–539PubMedGoogle Scholar
  61. 61.
    Wu CC, Hwang CR, Liu TJ, et al. Effects and limitations of prolonged intermittent ischaemia for hepatic resection of the cirrhotic liver. Br J Surg 1996;83:121–124PubMedGoogle Scholar
  62. 62.
    Cherqui D, Husson E, Hammoud R, et al. Laparoscopic liver resections: a feasibility study in 30 patients. Ann Surg 2000;232:753–762PubMedGoogle Scholar
  63. 63.
    Wu CC, Ho WL, Lin MC, et al. Is hepatic resection absolutely contraindicated for hepatocellular carcinoma in Child-Pugh class C cirrhotic patients? Hepatogastroenterology 1999;46:635–639PubMedGoogle Scholar
  64. 64.
    Yamamoto J, Kosuge T, Shimada K, et al. Anterior transhepatic approach for isolated resection of the caudate lobe of the liver. World J Surg 1999;23:97–101PubMedGoogle Scholar
  65. 65.
    Descottes B, Lachachi F, Sodji M, et al. Early experience with laparoscopic approach for solid liver tumors: initial 16 cases. Ann Surg 2000;232:641–645PubMedGoogle Scholar
  66. 66.
    Makuuchi M, Hasegawa H, Yamazaki S. Ultrasonically guided subsegmentectomy. Surg. Gynecol. Obstet. 1985;161:346–350PubMedGoogle Scholar
  67. 67.
    Horgan PG, Leen E. A simple technique for vascular control during hepatectomy: the half-Pringle. Am J Surg 2001;182:265–267CrossRefPubMedGoogle Scholar
  68. 68.
    Losanoff JE, Richman BW, Jones JW. The “half Pringle” maneuver. Am J Surg 2002;184:182–183PubMedGoogle Scholar
  69. 69.
    Ezaki T, Kanematsu T, Matsumata T, et al. Hemihepatic vascular occlusion using intraoperative ultrasonography: a simple technique. Br J Surg 1992;79:810PubMedGoogle Scholar
  70. 70.
    Makuuchi M, Mori T, Gunvén P, et al. Safety of hemihepatic vascular occlusion during resection of the liver. Surg. Gynecol. Obstet. 1987;164:155–158PubMedGoogle Scholar
  71. 71.
    Yanaga K, Matsumata T, Nishizaki T, et al. Alternate hemihepatic vascular control technique for hepatic resection. Am J Surg 1993;165:365–366PubMedGoogle Scholar
  72. 72.
    Castaing D, Garden OJ, Bismuth H. Segmental liver resection using ultrasound-guided selective portal venous occlusion. Ann Surg 1989;210:20–23PubMedGoogle Scholar
  73. 73.
    Goseki N, Kato S, Takamatsu S, et al. Hepatic resection under the intermittent selective portal branch occlusion by balloon catheter. J Am Coll Surg 1994;179:673–678PubMedGoogle Scholar
  74. 74.
    Huguet C, Addario-Chieco P, Gavelli A, et al. Technique of hepatic vascular exclusion for extensive liver resection. Am J Surg 1992;163:602–605CrossRefPubMedGoogle Scholar
  75. 75.
    De Cosmo GA, Adducci E, Gualtieri EM. Haemodynamic and metabolic changes during major liver resection with use of hepatic total vascular exclusion. Int. Surg. 2000;85:243–247PubMedGoogle Scholar
  76. 76.
    Emre S, Schwartz ME, Katz E, et al. Liver resection under total vascular isolation: variations on a theme. Ann Surg 1992;217:15–19Google Scholar
  77. 77.
    Stephen MS, Gallagher PJ, Ross Sheil AG, et al. Hepatic resection with vascular isolation and routine supraceliac aortic clamping. Am J Surg 1996;171:351–355CrossRefPubMedGoogle Scholar
  78. 78.
    Hannoun L, Delriviére L, Gibbs P, et al. Major extended hepatic resections in diseased livers using hypothermic protection: preliminary results from the first 12 patients treated with this technique. J Am Coll Surg 1996;183:597–605PubMedGoogle Scholar
  79. 79.
    Yamaoka Y, Ozawa K, Kumada K, et al. Total vascular exclusion for hepatic resection in cirrhotic patients: application of venovenous bypass. Arch Surg 1992;127:276–280PubMedGoogle Scholar
  80. 80.
    Huguet C, Gavelli A. Total vascular exclusion for liver resection. Hepatogastroenterology 1998;45:368–369PubMedGoogle Scholar
  81. 81.
    Miyazaki M, Ito M, Nakagawa K, et al. Aggressive surgical resection for hepatic metastases involving the inferior vena cava. Am J Surg 1999;177:294–298CrossRefPubMedGoogle Scholar
  82. 82.
    Vaillant JC, Borie BC, Hannoun L. Hepatectomy with hypothermic perfusion of the liver. Hepatogastroenterology 1998;45:381–388PubMedGoogle Scholar
  83. 83.
    Azoulay D, Eshkenazy R, Andreani P, et al. In situ hypothermic perfusion of the liver versus standard total vascular exclusion for complex liver resection. Ann Surg 2005;241:277–285CrossRefPubMedGoogle Scholar
  84. 84.
    Emond J, Wachs ME, Renz JF, et al. Total vascular exclusion for major hepatectomy in patients with abnormal liver parenchyma. Arch Surg 1995;130:824–831PubMedGoogle Scholar
  85. 85.
    Grazi GL, Mazziotti A, Jovine E, et al. Total vascular exclusion of the liver during hepatic surgery: selective use, extensive use or abuse? Arch Surg 1997;132:1104–1109PubMedGoogle Scholar
  86. 86.
    Kusano T, Tamai O, Miyazato H, et al. Extracorporeal bypass using a centrifugal pump during resection of malignant liver tumors. Hepatogastroenterology 1999;46:2483–2489PubMedGoogle Scholar
  87. 87.
    Habib NA, Michail NE, Boyle T, et al. Resection of the inferior vena cava during hepatectomy for liver tumors. Br J Surg 1994;81:1023–1024PubMedGoogle Scholar
  88. 88.
    Okada Y, Nagino M, Kamiya J, et al. Diagnosis and treatment of inferior vena cava invasion by hepatic cancer. World J Surg 2003;27:689–694CrossRefPubMedGoogle Scholar
  89. 89.
    Kelly D, Emre S, Guy SR, et al. Resection of benign hepatic lesions with selective use of total vascular control. J Am Coll Surg 1996;183:113–116PubMedGoogle Scholar
  90. 90.
    Elias D, Dubé P, Bonvalot S, et al. Intermittent complete vascular exclusion of the liver during hepatectomy: technique and indications. Hepatogastroenterology 1998;45:389–395PubMedGoogle Scholar
  91. 91.
    Makuuchi M, Hasegawa H, Yamazaki S, et al. Four new hepatectomy procedures for resection of the right hepatic vein and preservation of the inferior right hepatic vein. Surg Gynecol Obstet 1987;164:69–72Google Scholar
  92. 92.
    Makuuchi M, Yamamoto J, Takayama T, et al. Extrahepatic division of the right hepatic vein in hepatectomy. Hepatogastroenterology 1991;38:176–179PubMedGoogle Scholar
  93. 93.
    Elias D, Lasser P, Debaene B, et al. Intermittent vascular exclusion of the liver (without vena cava clamping) during major hepatectomy. Br J Surg 1995;82:1535–1539PubMedGoogle Scholar
  94. 94.
    Smyrniotis V, Arkadopoulos N, Kehagias D, et al. Liver resection with repair of major hepatic veins. Am J Surg 2002;183:58–61PubMedGoogle Scholar

Copyright information

© Société Internationale de Chirurgie 2005

Authors and Affiliations

  • Vassilios Smyrniotis
    • 1
  • Charalampos Farantos
    • 1
  • Georgia Kostopanagiotou
    • 2
  • Nikolaos Arkadopoulos
    • 1
  1. 1.Second Department of SurgeryAthens University Medical School, Aretaieion HospitalGreece
  2. 2.Second Department of AnesthesiologyAthens University Medical School, Attikon General University HospitalHaidariGreece

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