Basic Techniques for Hepatic Resection by the Glissonean Approach

  • Jixiong Hu
  • Jiangsheng Huang
  • Xianling LiuEmail author
  • Zhongkun Zuo


Liver resection for the treatment of hepatocellular carcinoma has progressed greatly over the last 20 years. Notable advancements include increased utilization of parenchymal-preserving resections, better patient selection, use of associating liver partition and portal vein ligation for staged hepatectomy (ALPPS), use of 3D virtual resection and reconstruction technology, and improvements in perioperative management [1]. Because of these changes, the postoperative morbidity and mortality have significantly decreased [2, 3]. Even if like this, intraoperative severe hemorrhage still is a potentially lethal problem, especially in patients with HCC associated with cirrhosis [4, 5]. Moreover, perioperative blood transfusion has been found to negatively influence long-term overall and disease-free survival [6, 7]. Therefore, minimizing blood loss while performing oncologically sound hepatectomy should be the primary goals of hepatic surgeons. During liver resection, blood loss occurs due to bleeding both from the vascular inflow system and from the vascular outflow system. It is similarly crucial to occlude the inflow and outflow systems to minimize bleeding during hepatic resection.


  1. 1.
    Kingham TP, Correagallego C, D’Angelica MI, Gönen M, Dematteo RP, Fong Y, Allen PJ, Blumgart LH, Jarnagin WR. Hepatic parenchymal preservation surgery: decreasing morbidity and mortality rates in 4,152 resections for malignancy. J Am Coll Surg. 2015;220(4):471–9.CrossRefGoogle Scholar
  2. 2.
    Zimmitti G, Roses RE, Andreou A, Shindoh J, Curley SA, Aloia TA, Vauthey JN. Greater complexity of liver surgery is not associated with an increased incidence of liver-related complications except for bile leak: an experience with 2,628 consecutive resections. Gastroenterology. 2013;17(1):57–65.Google Scholar
  3. 3.
    Sadamori H, Yagi T, Shinoura S, Umeda Y, Yoshida R, Satoh D, Nobuoka D, Utsumi M, Fujiwara T. Risk factors for major morbidity after liver resection for hepatocellular carcinoma. Br J Surg. 2013;100(1):122.CrossRefGoogle Scholar
  4. 4.
    Lau WY. A review on the operative techniques in liver resection. Chin Med J. 1997;110(7):567–70.PubMedGoogle Scholar
  5. 5.
    Müller MK, Petrowsky H, Clavien PA. Techniques of vascular control and protective strategies for parenchymal transection. Singapore: World Scientific Publishing; 2008.CrossRefGoogle Scholar
  6. 6.
    Kooby DA, Stockman J, Ben-Porat L, Gonen M, Jarnagin WR, Dematteo RP, Tuorto S, Wuest D, Blumgart LH, Fong Y. Influence of transfusions on perioperative and long-term outcome in patients following hepatic resection for colorectal metastases. Ann Surg. 2003;241(2):860–9.Google Scholar
  7. 7.
    Stephenson KR, Steinberg SM, Hughes KS, Vetto JT, Sugarbaker PH, Chang AE. Perioperative blood transfusions are associated with decreased time to recurrence and decreased survival after resection of colorectal liver metastases. Ann Surg. 1988;208(6):679.CrossRefGoogle Scholar
  8. 8.
    Pringle JH. Notes on the arrest of hepatic hemorrhage due to trauma. Ann Surg. 1908;48(4):541.CrossRefGoogle Scholar
  9. 9.
    Lowe MC, D’Angelica MI. Anatomy of hepatic resectional surgery. Surg Clin North Am. 2016;96(2):183.CrossRefGoogle Scholar
  10. 10.
    Belghiti J, Marty J, Farges O. Techniques, hemodynamic monitoring, and indications for vascular clamping during liver resections. J Hepatobiliary Pancreat Sci. 1998;5(1):69.CrossRefGoogle Scholar
  11. 11.
    Lau WY, et al. Chapter 9. Hepatic vascular inflow and outflow occlusion. In: Lau WY, editor. Applied anatomy in liver resection and liver transplantation. Beijing: People’s Medical Publishing House; 2011. p. 77–92.Google Scholar
  12. 12.
    Clavien PA, Yadav S, Sindram D, Bentley RC. Protective effects of ischemic preconditioning for liver resection performed under inflow occlusion in humans. Ann Surg. 2000;232(2):155.CrossRefGoogle Scholar
  13. 13.
    Clavien PA, Selzner M, Rüdiger HA, Graf R, Kadry Z, Rousson V, Jochum W. A prospective randomized study in 100 consecutive patients undergoing major liver resection with versus without ischemic preconditioning. Ann Surg. 2003;238(6):843.CrossRefGoogle Scholar
  14. 14.
    Chouker A, Schachtner TR, Dugas M, Lohe F, Martignoni A, Pollwein B, Niklas M, Rau HG, Jauch KW, Peter K. Effects of Pringle manoeuvre and ischaemic preconditioning on haemodynamic stability in patients undergoing elective hepatectomy: a randomized trial. Br J Anaesth. 2004;93(2):204.CrossRefGoogle Scholar
  15. 15.
    Heizmann O, Loehe F, Volk A, Schauer RJ. Ischemic preconditioning improves postoperative outcome after liver resections: a randomized controlled study. Eur J Med Res. 2008;13(2):79–86.PubMedGoogle Scholar
  16. 16.
    Li SQ, Liang LJ, Huang JF, Li Z. Ischemic preconditioning protects liver from hepatectomy under hepatic inflow occlusion for hepatocellular carcinoma patients with cirrhosis. World J Gastroenterol. 2004;10(17):2580.CrossRefGoogle Scholar
  17. 17.
    Makuuchi M, Mori T, Gunvén P, Yamazaki S, Hasegawa H. Safety of hemihepatic vascular occlusion during resection of the liver. Surg Gynecol Obstet. 1987;164(2):155.PubMedGoogle Scholar
  18. 18.
    Ken TMD. Glissonean pedicle transection method for hepatic resection. Tokyo: Springer; 2007.Google Scholar
  19. 19.
    Heaney JP, Stanton WK, Halbert DS, Seidel J, Vice T. An improved technic for vascular isolation of the liver: experimental study and case reports. Ann Surg. 1966;163(2):237.CrossRefGoogle Scholar
  20. 20.
    Lau WY, et al. Chapter 6. Intrahepatic Glissonian triad: anatomy relevant to liver resection and liver transplantation. In: Lau WY, editor. Applied anatomy in liver resection and liver transplantation. Beijing: People’s Medical Publishing House; 2011. p. 45–59.Google Scholar
  21. 21.
    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 J Surg. 2008;32(6):1082–7.CrossRefGoogle Scholar
  22. 22.
    Ueno M, Kawai M, Hayami S, Hirono S, Okada KI, Uchiyama K, Yamaue H. Partial clamping of the infrahepatic inferior vena cava for blood loss reduction during anatomic liver resection: a prospective, randomized, controlled trial. Surgery. 2017;161(6):1502–13.CrossRefGoogle Scholar
  23. 23.
    Hamady Z, Toogood G. Infrahepatic inferior vena cava clamping for reduction of central venous pressure and blood loss during hepatic resection: a randomized controlled trial. Ann Surg. 2011;253(6):1102–10.CrossRefGoogle Scholar
  24. 24.
    Otsubo T, Takasaki K, Yamamoto M, Katsuragawa H, Katagiri S, Yoshitoshi K, Hamano M, Ariizumi S, Kotera Y. Bleeding during hepatectomy can be reduced by clamping the inferior vena cava below the liver. Surgery. 2004;135(1):67–73.CrossRefGoogle Scholar
  25. 25.
    Chen XP, Zhang ZW, Zhang BX, Chen YF, Huang ZY, Zhang WG, He SQ, Qiu FZ. Modified technique of hepatic vascular exclusion: effect on blood loss during complex mesohepatectomy in hepatocellular carcinoma patients with cirrhosis. Langenbecks Arch Surg. 2006;391(3):209–15.CrossRefGoogle Scholar
  26. 26.
    Bismuth H, Castaing D, Garden OJ. Major hepatic resection under total vascular exclusion. Ann Surg. 1989;210(1):13.CrossRefGoogle Scholar
  27. 27.
    Smyrniotis V, Farantos C, Kostopanagiotou G, Arkadopoulos N. Vascular control during hepatectomy: review of methods and results. World J Surg. 2005;29(11):1384–96.CrossRefGoogle Scholar
  28. 28.
    Fu SY, Lau WY, Li AJ, Yang Y, Pan ZY, Sun YM, Lai ECH, Zhou WP, Wu MC. Liver resection under total vascular exclusion with or without preceding Pringle manoeuvre. Br J Surg. 2010;97(1):50.CrossRefGoogle Scholar
  29. 29.
    Fu SY, Lai EC, Li AJ, Pan ZY, Yang Y, Sun YM, Lau WY, Wu MC, Zhou WP. Liver resection with selective hepatic vascular exclusion: a cohort study. Ann Surg. 2009;249(4):624.CrossRefGoogle Scholar
  30. 30.
    Li AJ, Pan ZY, Zhou WP, Fu SY, Yang Y, Huang G, Yin L, Wu MC. Comparison of two methods of selective hepatic vascular exclusion for liver resection involving the roots of the hepatic veins. J Gastrointest Surg. 2008;12(8):1383–90.CrossRefGoogle Scholar
  31. 31.
    Zhou W, Li A, Pan Z, Fu S, Yang Y, Tang L, Hou Z, Wu M. Selective hepatic vascular exclusion and Pringle maneuver: a comparative study in liver resection. Eur J Surg Oncol. 2008;34(1):49–54.CrossRefGoogle Scholar
  32. 32.
    Miao XY, Hu JX, Dai WD, Zhong DW, Huang SF, Wen Y, Xiong SZ. Anatomic mesohepatectomy with extrahepatic control of hepatic veins. Hepatogastroenterology. 2009;56(96):1730–4.PubMedGoogle Scholar
  33. 33.
    Wen Y, Miao XY, Xiong L, Xiong G, Hu JX, Zhong DW, Li QL, Liu W. Application of hemihepatic vascular occlusion with hanging maneuver in hepatectomy. Hepato-gastroenterology. 2009;56(90):442–7.PubMedGoogle Scholar
  34. 34.
    Kang KJ, Ahn KS. Anatomical resection of hepatocellular carcinoma: a critical review of the procedure and its benefits on survival. World J Gastroenterol. 2017;23(7):1139–46.CrossRefGoogle Scholar
  35. 35.
    Fattovich G, Giustina G, Degos F, Tremolada F, Diodati G, Almasio P, Nevens F, Solinas A, Mura D, Brouwer JT. Morbidity and mortality in compensated cirrhosis type C: a retrospective follow-up study of 384 patients. Gastroenterology. 1997;112(2):463–72.CrossRefGoogle Scholar
  36. 36.
    Chen MF, Tsai HP, Jeng LB, Lee WC, Yeh CN, Yu MC, Hun CM. Prognostic factors after resection for hepatocellular carcinoma in noncirrhotic livers: univariate and multivariate analysis. World J Surg. 2003;27(4):443–7.CrossRefGoogle Scholar
  37. 37.
    Hasegawa K, Makuuchi M, Takayama T, Kokudo N, Arii S, Okazaki M, Okita K, Omata M, Kudo M, Kojiro M. Surgical resection vs. percutaneous ablation for hepatocellular carcinoma: a preliminary report of the Japanese nationwide survey. J Hepatol. 2008;50(4):589–94.CrossRefGoogle Scholar
  38. 38.
    Schroeder RA, Marroquin CE, Bute BP, Khuri S, Henderson WG, Kuo PC. Predictive indices of morbidity and mortality after liver resection. Ann Surg. 2006;243(3):373–9.CrossRefGoogle Scholar
  39. 39.
    Matsui Y, Terakawa N, Satoi S, Kaibori M, Kitade H, Takai S, Kwon AH, Kamiyama Y. Postoperative outcomes in patients with hepatocellular carcinomas resected with exposure of the tumor surface: clinical role of the no-margin resection. Arch Surg. 2007;142(7):596.CrossRefGoogle Scholar
  40. 40.
    Hasegawa K, Kokudo N, Imamura H, Matsuyama Y, Aoki T, Minagawa M, Sano K, Sugawara Y, Takayama T, Makuuchi M. Prognostic impact of anatomic resection for hepatocellular carcinoma. Ann Surg. 2005;242(2):252–9.CrossRefGoogle Scholar
  41. 41.
    Makuuchi M, Hasegawa H, Yamazaki S. Intraoperative ultrasonic examination for hepatectomy. Ultrasound Med Biol. 1981;11(2):493–7.Google Scholar
  42. 42.
    Couinaud C. Surgical anatomy of the liver revisited. Paris: Self-printed; 1989.Google Scholar
  43. 43.
    Couinaud CM. A simplified method for controlled left hepatectomy. Surgery. 1985;97(3):358–61.PubMedGoogle Scholar
  44. 44.
    Takasaki K, Kobayashi S, Tanaka S, Saito A, Yamamoto M, Hanyu F. Highly anatomically systematized hepatic resection with Glissonean sheath code transection at the hepatic hilus. Int Surg. 1990;75(2):73–7.PubMedGoogle Scholar
  45. 45.
    Sugioka A, Kato Y, Tanahashi Y. Systematic extrahepatic Glissonean pedicle isolation for anatomical liver resection based on Laennec’s capsule: proposal of a novel comprehensive surgical anatomy of the liver. J Hepatobiliary Pancreat Sci. 2017;24(1):17–23.CrossRefGoogle Scholar
  46. 46.
    Yamamoto M, Katagiri S, Ariizumi S, Kotera Y, Takahashi Y. Glissonean pedicle transection method for liver surgery (with video). J Hepatobiliary Pancreat Sci. 2012;19(1):3–8.CrossRefGoogle Scholar
  47. 47.
    Bernard L, Knoon HT. Chapter 19. Intrahepatic Glissonian approach. In: Lau WY, editor. Hepatocellular carcinoma. Singapore: World Scientific Publishing; 2008. p. 429–46.Google Scholar
  48. 48.
    Doklestić K, Djukić V, Bumbasirević V, Jovanović B, Karamarković A. Segment-oriented liver resections based on posterior intrahepatic Glissonian approach. Acta Chir Iugosl. 2012;59(3):41–8.CrossRefGoogle Scholar
  49. 49.
    Figueroa R, Laurenzi A, Laurent A, Cherqui D. Perihilar Glissonian approach for anatomical parenchymal sparing liver resections: technical aspects: the taping game. Ann Surg. 2016;267(3):537–43.CrossRefGoogle Scholar
  50. 50.
    Dai WD, Hu JX, Miao XY, Zhong DW, Wen Y, Xiong SZ. Intrahepatic Glissonian access for mesohepatectomy in cirrhotic patients. Hepatogastroenterology. 2008;55(85):1153–7.PubMedGoogle Scholar
  51. 51.
    Hu JX, Dai WD, Miao XY, Zhong DW, Huang SF, Wen Y, Xiong SZ. Anatomic resection of segment VIII of liver for hepatocellular carcinoma in cirrhotic patients based on an intrahepatic Glissonian approach. Surgery. 2009;146(5):854–60.CrossRefGoogle Scholar
  52. 52.
    Makuuchi M, Hasegawa H, Yamazaki S. Ultrasonically guided subsegmentectomy. Surg Gynecol Obstet. 1985;161(4):346.PubMedGoogle Scholar
  53. 53.
    Torzilli G, Procopio F, Cimino M, Del Fabbro D, Palmisano A, Donadon M, Montorsi M. Anatomical segmental and subsegmental resection of the liver for hepatocellular carcinoma. Ann Surg. 2009;251(2):229–35.CrossRefGoogle Scholar
  54. 54.
    Takasaki K, Kobayashi S, Tanaka S, Muto H, Watayo T, Saito A. Newly developed systematized hepatectomy by Glissonean pedicle transection method. Shujutsu. 1986;40:7–14. (in Japanese).Google Scholar
  55. 55.
    Fischer L, Cardenas C, Thorn M, Benner A, Grenacher L, Vetter M, Lehnert T, Klar E, Meinzer HP, Lamadã W. Limits of Couinaud’s liver segment classification: a quantitative computer-based three-dimensional analysis. J Comput Assist Tomogr. 2002;26(6):962–7.CrossRefGoogle Scholar
  56. 56.
    Shindoh J, Mise Y, Satou S, Sugawara Y, Kokudo N. The intersegmental plane of the liver is not always flat – tricks for anatomical liver resection. Ann Surg. 2010;251(5):917.CrossRefGoogle Scholar
  57. 57.
    Shouwang C, Shizhong Y, Wenping L, Geng C, Wanqing G, Weidong D, Weiyi W, Zhiqiang H, Jiahong D. Sustained methylene blue staining to guide anatomic hepatectomy for hepatocellular carcinoma: initial experience and technical details. Surgery. 2015;158(1):121–7.CrossRefGoogle Scholar
  58. 58.
    Lau WY, et al. Intrahepatic Glissonian approach. In: Lau WY, editor. Hepatocellular carcinoma. London: World Scientific Publishing; 2008. p. 429–46.CrossRefGoogle Scholar
  59. 59.
    Lau WY, et al. Intrahepatic Glissonian triad: anatomy relevant to liver resection and liver transplantation. In: Lau WY, editor. Applied anatomy in liver resection and liver transplantation. Beijing: People’s Medical Publishing House; 2010. p. 45–59.Google Scholar
  60. 60.
    Terminology Committee of the IHPBA. The Brisbane terminology of the liver anatomy and resection. HPB (Oxford). 2000;2:333–9.CrossRefGoogle Scholar
  61. 61.
    Yamamoto M, Katagiri S, Ariizumi S, Kotera Y, Takahashi Y, Egawa H. Tips for anatomical hepatectomy for hepatocellular carcinoma by the Glissonean pedicle approach (with videos). J Hepatobiliary Pancreat Sci. 2014;21(8):E53–6.CrossRefGoogle Scholar
  62. 62.
    Lortat-Jacob JL, Robert HG. Hepatectomie droite reglee. Presse Med. 1952;60:549–51.PubMedGoogle Scholar
  63. 63.
    Bismuth H. Surgical anatomy and anatomical surgery of the liver. World J Surg. 1982;6(1):3–9.CrossRefGoogle Scholar
  64. 64.
    Launois B, Jamieson GG. The importance of Glisson’s capsule and its sheath in the intrahepatic approach to resection of the liver. Surg Gynecol Obstet. 1992;174(1):7–10.PubMedGoogle Scholar
  65. 65.
    Katagiri S, Ariizumi SI, Kotera Y, Takahashi Y, Yamamoto M. Right hepatectomy using Glissonean pedicle transection method with anterior approach (with video). J Hepatobiliary Pancreat Sci. 2012;19(1):25–9.CrossRefGoogle Scholar
  66. 66.
    Yamanaka J, Fujimoto J. Sectionectomy of the liver. J Hepatobiliary Pancreat Sci. 2012;19(1):54.CrossRefGoogle Scholar
  67. 67.
    Yoshida H, Yu K, Rikiyama T, Motoi F, Onogawa T, Egawa S, Unno M. Segmentectomy of the liver. J Hepatobiliary Pancreat Sci. 2012;19(1):67–71.CrossRefGoogle Scholar
  68. 68.
    Couinaud C. Liver anatomy: a half century investigation. In: Forni E, Mernigi F, editors. Selected topics of HPB surgery and medicine. Pavia: IRCCS; 1995. p. 33–50.Google Scholar
  69. 69.
    Belghiti J, Guevara OA, Noun R, Saldinger PF, Kianmanesh R. Liver hanging maneuver: a safe approach to right hepatectomy without liver mobilization. J Am Coll Surg. 2001;193(1):109.CrossRefGoogle Scholar
  70. 70.
    Maddern GJ, Manganas D, Launois B. Clinical experience with the intrahepatic posterior approach to the portal triad for right hepatectomy and right segmental resection. World J Surg. 1995;19(5):764–7.CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Jixiong Hu
    • 1
  • Jiangsheng Huang
    • 2
  • Xianling Liu
    • 3
    Email author
  • Zhongkun Zuo
    • 2
  1. 1.Department of Hepatobiliary Surgery and Hunan Provincial Key Laboratory of Hepatobiliary Disease ResearchThe Second Xiangya Hospital, Central South UniversityChangshaPR China
  2. 2.Department of Minimally Invasive SurgeryThe Second Xiangya Hospital, Central South UniversityChangshaPR China
  3. 3.Department of OncologyThe Second Xiangya Hospital, Central South UniversityChangshaPR China

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