Skip to main content
Log in

Defining Post Hepatectomy Liver Insufficiency: Where do We stand?

  • Review Article
  • Published:
Journal of Gastrointestinal Surgery Aims and scope

Abstract

Background

Post-hepatectomy liver failure (PHLF) is a major source of morbidity and mortality in patients undergoing liver resection. The aim of this review is to summarize the recent literature available on PHLF including its definition, predictive factors, preoperative risk assessment, severity grading, preventative measures, and management strategies.

Methods

A systematic literature search was carried out with the search engines PubMed, Medline, and Cochrane Database using the keywords related to “liver failure”, “posthepatectomy”, and “hepatic resection”.

Results

Liver resection is a curative treatment of liver tumors. However, it leads to concurrent death and regeneration of the remaining hepatocytes. Factors related to the patient, liver parenchyma and the extent of surgery can inhibit regeneration leading to PHLF.

Conclusion

Given its resistance to treatment and the high postoperative mortality associated with PHLF, great effort has been put in to both accurately identify patients at high risk and to develop strategies that can help prevent its occurrence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Silberhumer GR, Paty PB, Temple LK, Araujo RL, Denton B, Gonen M, Nash GM, Allen PJ, DeMatteo RP, Guillem J, Weiser MR, D'Angelica MI, Jarnagin WR, D WW, Fong Y. Simultaneous resection for rectal cancer with synchronous liver metastasis is a safe procedure. Am J Surg. 2014.

  2. Imamura H, Seyama Y, Kokudo N, Aoki T, Sano K, Minagawa M, Sugawara Y, Makuuchi M. Single and multiple resections of multiple hepatic metastases of colorectal origin. Surgery 2004;135:508–17.

    Article  PubMed  Google Scholar 

  3. Spolverato G, Kim Y, Alexandrescu S, Popescu I, Marques HP, Aldrighetti L, Clark Gamblin T, Miura J, Maithel SK, Squires MH, Pulitano C, Sandroussi C, Mentha G, Bauer TW, Newhook T, Shen F, Poultsides GA, Wallis Marsh J, Pawlik TM. Is Hepatic Resection for Large or Multifocal Intrahepatic Cholangiocarcinoma Justified? Results from a Multi-Institutional Collaboration. Ann Surg Oncol. 2014.

  4. van den Broek MA, Olde Damink SW, Dejong CH, Lang H, Malago M, Jalan R, Saner FH. Liver failure after partial hepatic resection: definition, pathophysiology, risk factors and treatment. Liver Int. 2008;28:767–80.

    Article  PubMed  CAS  Google Scholar 

  5. Rahbari NN, Garden OJ, Padbury R, Brooke-Smith M, Crawford M, Adam R, Koch M, Makuuchi M, Dematteo RP, Christophi C, Banting S, Usatoff V, Nagino M, Maddern G, Hugh TJ, Vauthey JN, Greig P, Rees M, Yokoyama Y, Fan ST, Nimura Y, Figueras J, Capussotti L, Buchler MW, Weitz J. Posthepatectomy liver failure: a definition and grading by the International Study Group of Liver Surgery (ISGLS). Surgery. 2011;149:713–24.

    Article  PubMed  Google Scholar 

  6. Schreckenbach T, Liese J, Bechstein WO, Moench C. Posthepatectomy liver failure. Dig Surg. 2012;29:79–85.

    Article  PubMed  Google Scholar 

  7. Ribeiro HS, Costa WL, Jr., Diniz AL, Godoy AL, Herman P, Coudry RA, Begnami MD, Mello CA, Silva MJ, Zurstrassen CE, Coimbra FJ. Extended preoperative chemotherapy, extent of liver resection and blood transfusion are predictive factors of liver failure following resection of colorectal liver metastasis. Eur J Surg Oncol. 2013;39:380–5.

    Article  CAS  PubMed  Google Scholar 

  8. Filicori F, Keutgen XM, Zanello M, Ercolani G, Di Saverio S, Sacchetti F, Pinna AD, Grazi GL. Prognostic criteria for postoperative mortality in 170 patients undergoing major right hepatectomy. Hepatobiliary Pancreat Dis Int. 2012;11:507–12.

    Article  CAS  PubMed  Google Scholar 

  9. Kamiyama T, Nakanishi K, Yokoo H, Kamachi H, Tahara M, Kakisaka T, Tsuruga Y, Todo S, Taketomi A. Analysis of the risk factors for early death due to disease recurrence or progression within 1 year after hepatectomy in patients with hepatocellular carcinoma. World J Surg Oncol. 2012;10:107.

    Article  PubMed Central  PubMed  Google Scholar 

  10. Ren Z, Xu Y, Zhu S. Indocyanine green retention test avoiding liver failure after hepatectomy for hepatolithiasis. Hepatogastroenterology. 2012;59:782–4.

    PubMed  Google Scholar 

  11. Helling TS. Liver failure following partial hepatectomy. HPB (Oxford). 2006;8:165–74.

    Article  PubMed Central  PubMed  Google Scholar 

  12. Bolder U, Brune A, Schmidt S, Tacke J, Jauch KW, Lohlein D. Preoperative assessment of mortality risk in hepatic resection by clinical variables: a multivariate analysis. Liver Transpl Surg. 1999;5:227–37.

    Article  CAS  PubMed  Google Scholar 

  13. Simmonds PC, Primrose JN, Colquitt JL, Garden OJ, Poston GJ, Rees M. Surgical resection of hepatic metastases from colorectal cancer: a systematic review of published studies. Br J Cancer. 2006;94:982–99.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Timchenko NA. Aging and liver regeneration. Trends Endocrinol Metab. 2009;20:171–6.

    Article  CAS  PubMed  Google Scholar 

  15. Iakova P, Awad SS, Timchenko NA. Aging reduces proliferative capacities of liver by switching pathways of C/EBPalpha growth arrest. Cell. 2003;113:495–506.

    Article  CAS  PubMed  Google Scholar 

  16. Simon-Santamaria J, Malovic I, Warren A, Oteiza A, Le Couteur D, Smedsrod B, McCourt P, Sorensen KK. Age-related changes in scavenger receptor-mediated endocytosis in rat liver sinusoidal endothelial cells. J Gerontol A Biol Sci Med Sci. 2010;65:951–60.

    Article  PubMed  CAS  Google Scholar 

  17. Le Couteur DG, Warren A, Cogger VC, Smedsrod B, Sorensen KK, De Cabo R, Fraser R, McCuskey RS. Old age and the hepatic sinusoid. Anat Rec (Hoboken). 2008;291:672–83.

    Article  PubMed  Google Scholar 

  18. Balzan S, Belghiti J, Farges O, Ogata S, Sauvanet A, Delefosse D, Durand F. The "50-50 criteria" on postoperative day 5: an accurate predictor of liver failure and death after hepatectomy. Ann Surg. 2005;242:824–8, discussion 8–9.

    Article  PubMed Central  PubMed  Google Scholar 

  19. Mullen JT, Ribero D, Reddy SK, Donadon M, Zorzi D, Gautam S, Abdalla EK, Curley SA, Capussotti L, Clary BM, Vauthey JN. Hepatic insufficiency and mortality in 1,059 noncirrhotic patients undergoing major hepatectomy. J Am Coll Surg. 2007;204:854–62; discussion 62–4.

    Article  PubMed  Google Scholar 

  20. Aldrighetti L, Arru M, Caterini R, Finazzi R, Comotti L, Torri G, Ferla G. Impact of advanced age on the outcome of liver resection. World J Surg. 2003;27:1149–54.

    Article  PubMed  Google Scholar 

  21. Nanashima A, Abo T, Nonaka T, Fukuoka H, Hidaka S, Takeshita H, Ichikawa T, Sawai T, Yasutake T, Nakao K, Nagayasu T. Prognosis of patients with hepatocellular carcinoma after hepatic resection: are elderly patients suitable for surgery? J Surg Oncol. 2011;104:284–91.

    Article  PubMed  Google Scholar 

  22. Kim JM, Cho BI, Kwon CH, Joh JW, Park JB, Lee JH, Kim SJ, Paik SW, Park CK. Hepatectomy is a reasonable option for older patients with hepatocellular carcinoma. Am J Surg. 2015;209:391–7.

    Article  PubMed  Google Scholar 

  23. Little SA, Jarnagin WR, DeMatteo RP, Blumgart LH, Fong Y. Diabetes is associated with increased perioperative mortality but equivalent long-term outcome after hepatic resection for colorectal cancer. J Gastrointest Surg. 2002;6:88–94.

    Article  PubMed  Google Scholar 

  24. Bucher NL. Insulin, glucagon, and the liver. Adv Enzyme Regul. 1976;15:221–30.

    Article  CAS  PubMed  Google Scholar 

  25. Zarzavadjian Le Bian A, Costi R, Constantinides V, Smadja C. Metabolic disorders, non-alcoholic fatty liver disease and major liver resection: an underestimated perioperative risk. J Gastrointest Surg. 2012;16:2247–55.

  26. Huo TI, Lui WY, Huang YH, Chau GY, Wu JC, Lee PC, Chang FY, Lee SD. Diabetes mellitus is a risk factor for hepatic decompensation in patients with hepatocellular carcinoma undergoing resection: a longitudinal study. Am J Gastroenterol. 2003;98:2293–8.

    Article  PubMed  Google Scholar 

  27. Schindl MJ, Redhead DN, Fearon KC, Garden OJ, Wigmore SJ, Edinburgh Liver S, Transplantation Experimental Research G. The value of residual liver volume as a predictor of hepatic dysfunction and infection after major liver resection. Gut. 2005;54:289–96.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Fan ST, Lo CM, Lai EC, Chu KM, Liu CL, Wong J. Perioperative nutritional support in patients undergoing hepatectomy for hepatocellular carcinoma. N Engl J Med. 1994;331:1547–52.

    Article  CAS  PubMed  Google Scholar 

  29. Fan ST. Review: nutritional support for patients with cirrhosis. J Gastroenterol Hepatol. 1997;12:282–6.

    Article  CAS  PubMed  Google Scholar 

  30. Kaibori M, Inoue T, Sakakura Y, Oda M, Nagahama T, Kwon AH, Kamiyama Y, Miyazawa K, Okumura T. Impairment of activation of hepatocyte growth factor precursor into its mature form in rats with liver cirrhosis. J Surg Res. 2002;106:108–14.

    Article  CAS  PubMed  Google Scholar 

  31. Zhao G, Nakano K, Chijiiwa K, Ueda J, Tanaka M. Inhibited activities in CCAAT/enhancer-binding protein, activating protein-1 and cyclins after hepatectomy in rats with thioacetamide-induced liver cirrhosis. Biochem Biophys Res Commun. 2002;292:474–81.

    Article  CAS  PubMed  Google Scholar 

  32. Garcea G, Maddern GJ. Liver failure after major hepatic resection. J Hepatobiliary Pancreat Surg. 2009;16:145–55.

    Article  PubMed  Google Scholar 

  33. Bismuth H, Houssin D, Ornowski J, Meriggi F. Liver resections in cirrhotic patients: a Western experience. World J Surg. 1986;10:311–7.

    Article  CAS  PubMed  Google Scholar 

  34. Gozzetti G, Mazziotti A, Cavallari A, Bellusci R, Bolondi L, Grigioni W, Bragaglia R, Grazi GL, De Raffele E. Clinical experience with hepatic resections for hepatocellular carcinoma in patients with cirrhosis. Surg Gynecol Obstet. 1988;166:503–10.

    CAS  PubMed  Google Scholar 

  35. Capussotti L, Muratore A, Amisano M, Polastri R, Bouzari H, Massucco P. Liver resection for hepatocellular carcinoma on cirrhosis: analysis of mortality, morbidity and survival–a European single center experience. Eur J Surg Oncol. 2005;31:986–93.

    Article  CAS  PubMed  Google Scholar 

  36. Inaba Y, Furutani T, Kimura K, Watanabe H, Haga S, Kido Y, Matsumoto M, Yamamoto Y, Harada K, Kaneko S, Oyadomari S, Ozaki M, Kasuga M, Inoue H. Growth arrest and DNA damage-inducible 34 regulates liver regeneration in hepatic steatosis in mice. Hepatology. 2015;61:1343–56.

    Article  CAS  PubMed  Google Scholar 

  37. de Meijer VE, Kalish BT, Puder M, Ijzermans JN. Systematic review and meta-analysis of steatosis as a risk factor in major hepatic resection. Br J Surg. 2010;97:1331–9.

    Article  PubMed  Google Scholar 

  38. Reddy SK, Marsh JW, Varley PR, Mock BK, Chopra KB, Geller DA, Tsung A. Underlying steatohepatitis, but not simple hepatic steatosis, increases morbidity after liver resection: a case–control study. Hepatology. 2012;56:2221–30.

    Article  PubMed  Google Scholar 

  39. Vauthey JN, Pawlik TM, Ribero D, Wu TT, Zorzi D, Hoff PM, Xiong HQ, Eng C, Lauwers GY, Mino-Kenudson M, Risio M, Muratore A, Capussotti L, Curley SA, Abdalla EK. Chemotherapy regimen predicts steatohepatitis and an increase in 90-day mortality after surgery for hepatic colorectal metastases. J Clin Oncol. 2006;24:2065–72.

    Article  CAS  PubMed  Google Scholar 

  40. Robinson SM, Wilson CH, Burt AD, Manas DM, White SA. Chemotherapy-associated liver injury in patients with colorectal liver metastases: a systematic review and meta-analysis. Ann Surg Oncol. 2012;19:4287–99.

    Article  PubMed Central  PubMed  Google Scholar 

  41. Gomez D, Malik HZ, Bonney GK, Wong V, Toogood GJ, Lodge JP, Prasad KR. Steatosis predicts postoperative morbidity following hepatic resection for colorectal metastasis. Br J Surg. 2007;94:1395–402.

    Article  CAS  PubMed  Google Scholar 

  42. Tevar AD, Clarke C, Wang J, Rudich SM, Woodle ES, Lentsch AB, Edwards ML. Clinical review of nonalcoholic steatohepatitis in liver surgery and transplantation. J Am Coll Surg. 2010;210:515–26.

    Article  PubMed Central  PubMed  Google Scholar 

  43. Narita M, Oussoultzoglou E, Chenard MP, Rosso E, Casnedi S, Pessaux P, Bachellier P, Jaeck D. Sinusoidal obstruction syndrome compromises liver regeneration in patients undergoing two-stage hepatectomy with portal vein embolization. Surg Today. 2011;41:7–17.

    Article  PubMed  Google Scholar 

  44. Kubota K, Makuuchi M, Kusaka K, Kobayashi T, Miki K, Hasegawa K, Harihara Y, Takayama T. Measurement of liver volume and hepatic functional reserve as a guide to decision-making in resectional surgery for hepatic tumors. Hepatology. 1997;26:1176–81.

    CAS  PubMed  Google Scholar 

  45. 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;237:860–9; discussion 9–70.

    PubMed Central  PubMed  Google Scholar 

  46. Poon RT, Fan ST, Lo CM, Liu CL, Lam CM, Yuen WK, Yeung C, Wong J. Improving perioperative outcome expands the role of hepatectomy in management of benign and malignant hepatobiliary diseases: analysis of 1222 consecutive patients from a prospective database. Ann Surg. 2004;240:698–708; discussion −10.

  47. Imamura H, Seyama Y, Kokudo N, Maema A, Sugawara Y, Sano K, Takayama T, Makuuchi M. One thousand fifty-six hepatectomies without mortality in 8 years. Arch Surg. 2003;138:1198–206; discussion 206.

    Article  PubMed  Google Scholar 

  48. Silva MA, Muralidharan V, Mirza DF. The management of coagulopathy and blood loss in liver surgery. Semin Hematol. 2004;41:132–9.

    Article  PubMed  Google Scholar 

  49. Luyer MD, Buurman WA, Hadfoune M, Jacobs JA, Konstantinov SR, Dejong CH, Greve JW. Pretreatment with high-fat enteral nutrition reduces endotoxin and tumor necrosis factor-alpha and preserves gut barrier function early after hemorrhagic shock. Shock. 2004;21:65–71.

    Article  PubMed  Google Scholar 

  50. Jensen LS, Andersen AJ, Christiansen PM, Hokland P, Juhl CO, Madsen G, Mortensen J, Moller-Nielsen C, Hanberg-Sorensen F, Hokland M. Postoperative infection and natural killer cell function following blood transfusion in patients undergoing elective colorectal surgery. Br J Surg. 1992;79:513–6.

    Article  CAS  PubMed  Google Scholar 

  51. Kiuchi T, Kasahara M, Uryuhara K, Inomata Y, Uemoto S, Asonuma K, Egawa H, Fujita S, Hayashi M, Tanaka K. Impact of graft size mismatching on graft prognosis in liver transplantation from living donors. Transplantation. 1999;67:321–7.

    Article  CAS  PubMed  Google Scholar 

  52. Furukawa H, Kishida A, Omura T, Kamiyama T, Suzuki T, Matsushita M, Nakajima Y, Todo S. Indication and strategy for adult living related liver transplantation. Transplant Proc. 1999;31:1952.

    Article  CAS  PubMed  Google Scholar 

  53. Emond JC, Renz JF, Ferrell LD, Rosenthal P, Lim RC, Roberts JP, Lake JR, Ascher NL. Functional analysis of grafts from living donors. Implications for the treatment of older recipients. Ann Surg. 1996;224:544–52; discussion 52–4.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  54. Selzner N, Selzner M, Odermatt B, Tian Y, Van Rooijen N, Clavien PA. ICAM-1 triggers liver regeneration through leukocyte recruitment and Kupffer cell-dependent release of TNF-alpha/IL-6 in mice. Gastroenterology. 2003;124:692–700.

    Article  CAS  PubMed  Google Scholar 

  55. Akita K, Okuno M, Enya M, Imai S, Moriwaki H, Kawada N, Suzuki Y, Kojima S. Impaired liver regeneration in mice by lipopolysaccharide via TNF-alpha/kallikrein-mediated activation of latent TGF-beta. Gastroenterology. 2002;123:352–64.

    Article  CAS  PubMed  Google Scholar 

  56. Rice GC, Leiberman DP, Mathie RT, Ryan CJ, Harper AM, Blumgart LH. Liver tissue blood flow measured by 85Kr clearance in the anaesthetized rat before and after partial hepatectomy. Br J Exp Pathol. 1977;58:243–50.

    PubMed Central  CAS  PubMed  Google Scholar 

  57. Golse N, Bucur PO, Adam R, Castaing D, Sa Cunha A, Vibert E. New paradigms in post-hepatectomy liver failure. J Gastrointest Surg. 2013;17:593–605.

    Article  PubMed  Google Scholar 

  58. Schoen JM, Wang HH, Minuk GY, Lautt WW. Shear stress-induced nitric oxide release triggers the liver regeneration cascade. Nitric Oxide. 2001;5:453–64.

    Article  CAS  PubMed  Google Scholar 

  59. Michalopoulos GK. Liver regeneration. J Cell Physiol. 2007;213:286–300.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  60. Jin X, Zimmers TA, Perez EA, Pierce RH, Zhang Z, Koniaris LG. Paradoxical effects of short- and long-term interleukin-6 exposure on liver injury and repair. Hepatology. 2006;43:474–84.

    Article  CAS  PubMed  Google Scholar 

  61. Taub R. Liver regeneration: from myth to mechanism. Nat Rev Mol Cell Biol. 2004;5:836–47.

    Article  CAS  PubMed  Google Scholar 

  62. Wack KE, Ross MA, Zegarra V, Sysko LR, Watkins SC, Stolz DB. Sinusoidal ultrastructure evaluated during the revascularization of regenerating rat liver. Hepatology. 2001;33:363–78.

    Article  CAS  PubMed  Google Scholar 

  63. Nagasue N, Yukaya H, Ogawa Y, Kohno H, Nakamura T. Human liver regeneration after major hepatic resection. A study of normal liver and livers with chronic hepatitis and cirrhosis. Ann Surg. 1987;206:30–9.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  64. Panis Y, McMullan DM, Emond JC. Progressive necrosis after hepatectomy and the pathophysiology of liver failure after massive resection. Surgery. 1997;121:142–9.

    Article  CAS  PubMed  Google Scholar 

  65. Oussoultzoglou E, Jaeck D, Addeo P, Fuchshuber P, Marzano E, Rosso E, Pessaux P, Bachellier P. Prediction of mortality rate after major hepatectomy in patients without cirrhosis. Arch Surg. 2010;145:1075–81.

    Article  PubMed  Google Scholar 

  66. Maeda Y, Nishida M, Takao T, Mori N, Tamesa T, Tangoku A, Oka M. Risk factors for postoperative liver failure after hepatectomy for hepatocellular carcinoma. Hepatogastroenterology. 2004;51:1792–6.

    PubMed  Google Scholar 

  67. Osada S, Saji S. The clinical significance of monitoring alkaline phosphatase level to estimate postoperative liver failure after hepatectomy. Hepatogastroenterology. 2004;51:1434–8.

    PubMed  Google Scholar 

  68. Nanashima A, Tobinaga S, Abo T, Nonaka T, Takeshita H, Hidaka S, Sawai T, Nagayasu T. Reducing the incidence of post-hepatectomy hepatic complications by preoperatively applying parameters predictive of liver function. J Hepatobiliary Pancreat Sci. 2010;17:871–8.

    Article  PubMed  Google Scholar 

  69. Reissfelder C, Rahbari NN, Koch M, Kofler B, Sutedja N, Elbers H, Buchler MW, Weitz J. Postoperative course and clinical significance of biochemical blood tests following hepatic resection. Br J Surg. 2011;98:836–44.

    Article  CAS  PubMed  Google Scholar 

  70. Du ZG, Wei YG, Chen KF, Li B. An accurate predictor of liver failure and death after hepatectomy: a single institution's experience with 478 consecutive cases. World J Gastroenterol. 2014;20:274–81.

    Article  PubMed Central  PubMed  Google Scholar 

  71. Hotta T, Kobayashi Y, Taniguchi K, Johata K, Sahara M, Ochiai M, Watanabe T, Tanimura H. Liver functional analysis by total bile acid level of C-tube bile after hepatectomy. Hepatogastroenterology. 2005;52:1211–5.

    PubMed  Google Scholar 

  72. Yokoyama Y, Ebata T, Igami T, Sugawara G, Ando M, Nagino M. Predictive power of prothrombin time and serum total bilirubin for postoperative mortality after major hepatectomy with extrahepatic bile duct resection. Surgery. 2014;155:504–11.

    Article  PubMed  Google Scholar 

  73. Ercolani G, Grazi GL, Calliva R, Pierangeli F, Cescon M, Cavallari A, Mazziotti A. The lidocaine (MEGX) test as an index of hepatic function: its clinical usefulness in liver surgery. Surgery. 2000;127:464–71.

    Article  CAS  PubMed  Google Scholar 

  74. Delis SG, Bakoyiannis A, Dervenis C, Tassopoulos N. Perioperative risk assessment for hepatocellular carcinoma by using the MELD score. J Gastrointest Surg. 2009;13:2268–75.

    Article  PubMed  Google Scholar 

  75. Huang L, Li J, Yan JJ, Liu CF, Wu MC, Yan YQ. Prealbumin is predictive for postoperative liver insufficiency in patients undergoing liver resection. World J Gastroenterol. 2012;18:7021–5.

    Article  PubMed Central  PubMed  Google Scholar 

  76. Huo TI, Lui WY, Wu JC, Huang YH, King KL, Loong CC, Lee PC, Chang FY, Lee SD. Deterioration of hepatic functional reserve in patients with hepatocellular carcinoma after resection: incidence, risk factors, and association with intrahepatic tumor recurrence. World J Surg. 2004;28:258–62.

    Article  PubMed  Google Scholar 

  77. Wang Q, Lau WY, Zhang B, Zhang Z, Huang Z, Luo H, Chen X. Preoperative total cholesterol predicts postoperative outcomes after partial hepatectomy in patients with chronic hepatitis B- or C-related hepatocellular carcinoma. Surgery. 2014;155:263–70.

    Article  PubMed  Google Scholar 

  78. Cucchetti A, Ercolani G, Cescon M, Ravaioli M, Zanello M, Del Gaudio M, Lauro A, Vivarelli M, Grazi GL, Pinna AD. Recovery from liver failure after hepatectomy for hepatocellular carcinoma in cirrhosis: meaning of the model for end-stage liver disease. J Am Coll Surg. 2006;203:670–6.

    Article  PubMed  Google Scholar 

  79. Rahbari NN, Reissfelder C, Koch M, Elbers H, Striebel F, Buchler MW, Weitz J. The predictive value of postoperative clinical risk scores for outcome after hepatic resection: a validation analysis in 807 patients. Ann Surg Oncol. 2011;18:3640–9.

    Article  PubMed  Google Scholar 

  80. Hyder O, Pulitano C, Firoozmand A, Dodson R, Wolfgang CL, Choti MA, Aldrighetti L, Pawlik TM. A risk model to predict 90-day mortality among patients undergoing hepatic resection. J Am Coll Surg. 2013;216:1049–56.

    Article  PubMed Central  PubMed  Google Scholar 

  81. Teh SH, Nagorney DM, Stevens SR, Offord KP, Therneau TM, Plevak DJ, Talwalkar JA, Kim WR, Kamath PS. Risk factors for mortality after surgery in patients with cirrhosis. Gastroenterology. 2007;132:1261–9.

    Article  PubMed  Google Scholar 

  82. Hemming AW, Scudamore CH, Shackleton CR, Pudek M, Erb SR. Indocyanine green clearance as a predictor of successful hepatic resection in cirrhotic patients. Am J Surg. 1992;163:515–8.

    Article  CAS  PubMed  Google Scholar 

  83. Nonami T, Nakao A, Kurokawa T, Inagaki H, Matsushita Y, Sakamoto J, Takagi H. Blood loss and ICG clearance as best prognostic markers of post-hepatectomy liver failure. Hepatogastroenterology. 1999;46:1669–72.

    CAS  PubMed  Google Scholar 

  84. de Liguori Carino N, O'Reilly DA, Dajani K, Ghaneh P, Poston GJ, Wu AV. Perioperative use of the LiMON method of indocyanine green elimination measurement for the prediction and early detection of post-hepatectomy liver failure. Eur J Surg Oncol. 2009;35:957–62.

    Article  PubMed  Google Scholar 

  85. Ohwada S, Kawate S, Hamada K, Yamada T, Sunose Y, Tsutsumi H, Tago K, Okabe T. Perioperative real-time monitoring of indocyanine green clearance by pulse spectrophotometry predicts remnant liver functional reserve in resection of hepatocellular carcinoma. Br J Surg. 2006;93:339–46.

    Article  CAS  PubMed  Google Scholar 

  86. Yokoyama Y, Nishio H, Ebata T, Igami T, Sugawara G, Nagino M. Value of indocyanine green clearance of the future liver remnant in predicting outcome after resection for biliary cancer. Br J Surg. 2010;97:1260–8.

    Article  CAS  PubMed  Google Scholar 

  87. Derpapas MK, Contis J, Fragulidis GP, Lykoudis PM, Polymeneas G, Ntourakis S, Voros D. Correlation of the ICG test with risk factors and postoperative outcomes following hepatic resection. J buon. 2013;18:703–7.

    CAS  PubMed  Google Scholar 

  88. Scheingraber S, Richter S, Igna D, Flesch S, Kopp B, Schilling MK. Indocyanine green disappearance rate is the most useful marker for liver resection. Hepatogastroenterology. 2008;55:1394–9.

    CAS  PubMed  Google Scholar 

  89. Tralhao JG, Hoti E, Oliveiros B, Botelho MF, Sousa FC. Study of perioperative liver function by dynamic monitoring of ICG-clearance. Hepatogastroenterology. 2012;59:1179–83.

    CAS  PubMed  Google Scholar 

  90. Okochi O, Kaneko T, Sugimoto H, Inoue S, Takeda S, Nakao A. ICG pulse spectrophotometry for perioperative liver function in hepatectomy. J Surg Res. 2002;103:109–13.

    Article  PubMed  Google Scholar 

  91. Fan ST. Liver functional reserve estimation: state of the art and relevance for local treatments: the Eastern perspective. J Hepatobiliary Pancreat Sci. 2010;17:380–4.

    Article  PubMed  Google Scholar 

  92. Zipprich A, Kuss O, Rogowski S, Kleber G, Lotterer E, Seufferlein T, Fleig WE, Dollinger MM. Incorporating indocyanin green clearance into the Model for End Stage Liver Disease (MELD-ICG) improves prognostic accuracy in intermediate to advanced cirrhosis. Gut. 2010;59:963–8.

    Article  PubMed  Google Scholar 

  93. Fan ST, Lai EC, Lo CM, Ng IO, Wong J. Hospital mortality of major hepatectomy for hepatocellular carcinoma associated with cirrhosis. Arch Surg. 1995;130:198–203.

    Article  CAS  PubMed  Google Scholar 

  94. Lam CM, Fan ST, Lo CM, Wong J. Major hepatectomy for hepatocellular carcinoma in patients with an unsatisfactory indocyanine green clearance test. Br J Surg. 1999;86:1012–7.

    Article  CAS  PubMed  Google Scholar 

  95. Zoedler T, Ebener C, Becker H, Roeher HD. Evaluation of liver function tests to predict operative risk in liver surgery. HPB Surg. 1995;9:13–8.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  96. Fan ST, Wang QS, Lo CM, Tam Yu KW, Lai EC, Wong J. Evaluation of indocyanine green retention and aminopyrine breath tests in patients with malignant biliary obstruction. Aust N Z J Surg. 1994;64:759–62.

    Article  CAS  PubMed  Google Scholar 

  97. Caesar J, Shaldon S, Chiandussi L, Guevara L, Sherlock S. The use of indocyanine green in the measurement of hepatic blood flow and as a test of hepatic function. Clin Sci. 1961;21:43–57.

    CAS  PubMed  Google Scholar 

  98. Shirin H, Aeed H, Shalev T, Sorin V, Stavinski S, Shahmurov M, Ilan Y, Avni Y. Utility of a 13C-methacetin breath test in evaluating hepatic injury in rats. J Gastroenterol Hepatol. 2008;23:1762–8.

    Article  PubMed  Google Scholar 

  99. Yachida S, Wakabayashi H, Kokudo Y, Goda F, Okada S, Maeba T, Maeta H. Measurement of serum hyaluronate as a predictor of human liver failure after major hepatectomy. World J Surg. 2000;24:359–64.

    Article  CAS  PubMed  Google Scholar 

  100. Kubo S, Tsukamoto T, Hirohashi K, Tanaka H, Shuto T, Takemura S, Yamamoto T, Uenishi T, Ogawa M, Kinoshita H. Correlation between preoperative serum concentration of type IV collagen 7s domain and hepatic failure following resection of hepatocellular carcinoma. Ann Surg. 2004;239:186–93.

    Article  PubMed Central  PubMed  Google Scholar 

  101. Kiuchi T, Ozawa K, Yamamoto Y, Takayasu T, Maki A, Shimahara Y, Mori K, Kobayashi N, Yamaoka Y, Kumada K. Changes in arterial ketone body ratio in the phase immediately after hepatectomy. Prognostic implications. Arch Surg. 1990;125:655–9.

    Article  CAS  PubMed  Google Scholar 

  102. Yoshida M, Shiraishi S, Sakaguchi F, Utsunomiya D, Tashiro K, Tomiguchi S, Okabe H, Beppu T, Baba H, Yamashita Y. Fused 99m-Tc-GSA SPECT/CT imaging for the preoperative evaluation of postoperative liver function: can the liver uptake index predict postoperative hepatic functional reserve? Jpn J Radiol. 2012;30:255–62.

    Article  PubMed  Google Scholar 

  103. Katsuramaki T, Fujimori K, Furuhata T, Kimura Y, Meguro M, Nagayama M, Honma T, Mukaiya M, Hareyama M, Hirata K. Preoperative estimation of risk in hepatectomy using technetium-99m-galactosyl human serum albumin receptor amount by nonlinear 3-compartment model. Hepatogastroenterology. 2003;50:174–7.

    PubMed  Google Scholar 

  104. Kwon AH, Matsui Y, Kaibori M, Ha-Kawa SK. Preoperative regional maximal removal rate of technetium-99m-galactosyl human serum albumin (GSA-Rmax) is useful for judging the safety of hepatic resection. Surgery. 2006;140:379–86.

    Article  PubMed  Google Scholar 

  105. Kokudo N, Vera DR, Tada K, Koizumi M, Seki M, Matsubara T, Ohta H, Yamaguchi T, Takahashi T, Nakajima T, Muto T. Predictors of successful hepatic resection: prognostic usefulness of hepatic asialoglycoprotein receptor analysis. World J Surg. 2002;26:1342–7.

    Article  PubMed  Google Scholar 

  106. Kaibori M, Ha-Kawa SK, Ishizaki M, Matsui K, Saito T, Kwon AH, Kamiyama Y. HA/GSA-Rmax ratio as a predictor of postoperative liver failure. World J Surg. 2008;32:2410–8.

    Article  PubMed  Google Scholar 

  107. Thian YL, Riddell AM, Koh DM. Liver-specific agents for contrast-enhanced MRI: role in oncological imaging. Cancer Imaging. 2013;13:567–79.

    Article  PubMed Central  PubMed  Google Scholar 

  108. Wibmer A, Prusa AM, Nolz R, Gruenberger T, Schindl M, Ba-Ssalamah A. Liver failure after major liver resection: risk assessment by using preoperative Gadoxetic acid-enhanced 3-T MR imaging. Radiology. 2013;269:777–86.

    Article  PubMed  Google Scholar 

  109. Tsuboyama T, Onishi H, Kim T, Akita H, Hori M, Tatsumi M, Nakamoto A, Nagano H, Matsuura N, Wakasa K, Tomoda K. Hepatocellular carcinoma: hepatocyte-selective enhancement at gadoxetic acid-enhanced MR imaging–correlation with expression of sinusoidal and canalicular transporters and bile accumulation. Radiology. 2010;255:824–33.

    Article  PubMed  Google Scholar 

  110. D'Onofrio M, De Robertis R, Demozzi E, Crosara S, Canestrini S, Pozzi Mucelli R. Liver volumetry: Is imaging reliable? Personal experience and review of the literature. World J Radiol. 2014;6:62–71.

    Article  PubMed Central  PubMed  Google Scholar 

  111. Kitajima K, Taboury J, Boleslawski E, Savier E, Vaillant JC, Hannoun L. Sonographic preoperative assessment of liver volume before major liver resection. Gastroenterol Clin Biol. 2008;32:382–9.

    Article  CAS  PubMed  Google Scholar 

  112. Xu HX, Yin XY, Lu MD, Liu GJ, Xu ZF. Estimation of liver tumor volume using a three-dimensional ultrasound volumetric system. Ultrasound Med Biol. 2003;29:839–46.

    Article  PubMed  Google Scholar 

  113. Ulla M, Ardiles V, Levy-Yeyati E, Alvarez FA, Spina JC, Garcia-Monaco RD, De Santibanes E. New surgical strategy to induce liver hypertrophy: role of MDCT-volumetry to monitor and predict liver growth. Hepatogastroenterology. 2013;60:337–42.

    PubMed  Google Scholar 

  114. Yamanaka N, Okamoto E, Oriyama T, Fujimoto J, Furukawa K, Kawamura E, Tanaka T, Tomoda F. A prediction scoring system to select the surgical treatment of liver cancer. Further refinement based on 10 years of use. Ann Surg. 1994;219:342–6.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  115. Uchiyama K, Mori K, Tabuse K, Ueno M, Ozawa S, Nakase T, Kawai M, Tani M, Tanimura H, Yamaue H. Assessment of liver function for successful hepatectomy in patients with hepatocellular carcinoma with impaired hepatic function. J Hepatobiliary Pancreat Surg. 2008;15:596–602.

    Article  PubMed  Google Scholar 

  116. Du ZG, Li B, Wei YG, Yin J, Feng X, Chen X. A new scoring system for assessment of liver function after successful hepatectomy in patients with hepatocellular carcinoma. Hepatobiliary Pancreat Dis Int. 2011;10:265–9.

    Article  PubMed  Google Scholar 

  117. Ribero D, Chun YS, Vauthey JN. Standardized liver volumetry for portal vein embolization. Semin Intervent Radiol. 2008;25:104–9.

    Article  PubMed Central  PubMed  Google Scholar 

  118. Vauthey JN, Chaoui A, Do KA, Bilimoria MM, Fenstermacher MJ, Charnsangavej C, Hicks M, Alsfasser G, Lauwers G, Hawkins IF, Caridi J. Standardized measurement of the future liver remnant prior to extended liver resection: methodology and clinical associations. Surgery. 2000;127:512–9.

    Article  CAS  PubMed  Google Scholar 

  119. Abdalla EK, Adam R, Bilchik AJ, Jaeck D, Vauthey JN, Mahvi D. Improving resectability of hepatic colorectal metastases: expert consensus statement. Ann Surg Oncol. 2006;13:1271–80.

    Article  PubMed  Google Scholar 

  120. Ribero D, Abdalla EK, Madoff DC, Donadon M, Loyer EM, Vauthey JN. Portal vein embolization before major hepatectomy and its effects on regeneration, resectability and outcome. Br J Surg. 2007;94:1386–94.

    Article  CAS  PubMed  Google Scholar 

  121. Kishi Y, Abdalla EK, Chun YS, Zorzi D, Madoff DC, Wallace MJ, Curley SA, Vauthey JN. Three hundred and one consecutive extended right hepatectomies: evaluation of outcome based on systematic liver volumetry. Ann Surg. 2009;250:540–8.

    PubMed  Google Scholar 

  122. Skrzypczyk C, Truant S, Duhamel A, Langlois C, Boleslawski E, Koriche D, Hebbar M, Fourrier F, Mathurin P, Pruvot FR. Relevance of the ISGLS definition of posthepatectomy liver failure in early prediction of poor outcome after liver resection: study on 680 hepatectomies. Ann Surg. 2014;260:865–70; discussion 70.

    Article  PubMed  Google Scholar 

  123. McCormack L, Petrowsky H, Jochum W, Furrer K, Clavien PA. Hepatic steatosis is a risk factor for postoperative complications after major hepatectomy: a matched case–control study. Ann Surg. 2007;245:923–30.

    Article  PubMed Central  PubMed  Google Scholar 

  124. Roberts KJ, Bharathy KG, Lodge JP. Kinetics of liver function tests after a hepatectomy for colorectal liver metastases predict post-operative liver failure as defined by the International Study Group for Liver Surgery. HPB (Oxford). 2013;15:345–51.

    Article  PubMed Central  PubMed  Google Scholar 

  125. Yigitler C, Farges O, Kianmanesh R, Regimbeau JM, Abdalla EK, Belghiti J. The small remnant liver after major liver resection: how common and how relevant? Liver Transpl. 2003;9:S18-25.

    Article  PubMed  Google Scholar 

  126. Hemming AW, Reed AI, Howard RJ, Fujita S, Hochwald SN, Caridi JG, Hawkins IF, Vauthey JN. Preoperative portal vein embolization for extended hepatectomy. Ann Surg. 2003;237:686–91; discussion 91–3.

    PubMed Central  PubMed  Google Scholar 

  127. Kinoshita H, Sakai K, Hirohashi K, Igawa S, Yamasaki O, Kubo S. Preoperative portal vein embolization for hepatocellular carcinoma. World J Surg. 1986;10:803–8.

    Article  CAS  PubMed  Google Scholar 

  128. Makuuchi M, Thai BL, Takayasu K, Takayama T, Kosuge T, Gunven P, Yamazaki S, Hasegawa H, Ozaki H. Preoperative portal embolization to increase safety of major hepatectomy for hilar bile duct carcinoma: a preliminary report. Surgery. 1990;107:521–7.

    CAS  PubMed  Google Scholar 

  129. Abulkhir A, Limongelli P, Healey AJ, Damrah O, Tait P, Jackson J, Habib N, Jiao LR. Preoperative portal vein embolization for major liver resection: a meta-analysis. Ann Surg. 2008;247:49–57.

    Article  PubMed  Google Scholar 

  130. Adam R, Laurent A, Azoulay D, Castaing D, Bismuth H. Two-stage hepatectomy: A planned strategy to treat irresectable liver tumors. Ann Surg. 2000;232:777–85.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  131. Tsai S, Marques HP, de Jong MC, Mira P, Ribeiro V, Choti MA, Schulick RD, Barroso E, Pawlik TM. Two-stage strategy for patients with extensive bilateral colorectal liver metastases. HPB (Oxford). 2010;12:262–9.

    Article  PubMed Central  PubMed  Google Scholar 

  132. Pandanaboyana S, Bell R, Hidalgo E, Toogood G, Prasad KR, Bartlett A, Lodge JP. A systematic review and meta-analysis of portal vein ligation versus portal vein embolization for elective liver resection. Surgery. 2015;157:690–8.

    Article  PubMed  Google Scholar 

  133. Schnitzbauer AA, Lang SA, Goessmann H, Nadalin S, Baumgart J, Farkas SA, Fichtner-Feigl S, Lorf T, Goralcyk A, Horbelt R, Kroemer A, Loss M, Rummele P, Scherer MN, Padberg W, Konigsrainer A, Lang H, Obed A, Schlitt HJ. Right portal vein ligation combined with in situ splitting induces rapid left lateral liver lobe hypertrophy enabling 2-staged extended right hepatic resection in small-for-size settings. Ann Surg. 2012;255:405–14.

    Article  PubMed  Google Scholar 

  134. Zhang GQ, Zhang ZW, Lau WY, Chen XP. Associating liver partition and portal vein ligation for staged hepatectomy (ALPPS): a new strategy to increase resectability in liver surgery. Int J Surg. 2014;12:437–41.

    Article  PubMed  Google Scholar 

  135. Bernal W, Wendon J. Acute liver failure. N Engl J Med. 2013;369:2525–34.

    Article  CAS  PubMed  Google Scholar 

  136. Singanayagam A, Bernal W. Update on acute liver failure. Curr Opin Crit Care. 2015;21:134–41.

    Article  PubMed  Google Scholar 

  137. Chiu A, Chan LM, Fan ST. Molecular adsorbent recirculating system treatment for patients with liver failure: the Hong Kong experience. Liver Int. 2006;26:695–702.

    Article  CAS  PubMed  Google Scholar 

  138. Rahimi RS, Singal AG, Cuthbert JA, Rockey DC. Lactulose vs polyethylene glycol 3350–electrolyte solution for treatment of overt hepatic encephalopathy: the HELP randomized clinical trial. JAMA Intern Med. 2014;174:1727–33.

    Article  CAS  PubMed  Google Scholar 

  139. Mas A, Rodes J, Sunyer L, Rodrigo L, Planas R, Vargas V, Castells L, Rodriguez-Martinez D, Fernandez-Rodriguez C, Coll I, Pardo A, Spanish Association for the Study of the Liver Hepatic Encephalopathy Cooperative G. Comparison of rifaximin and lactitol in the treatment of acute hepatic encephalopathy: results of a randomized, double-blind, double-dummy, controlled clinical trial. J Hepatol. 2003;38:51–8.

    Article  CAS  PubMed  Google Scholar 

  140. Leithead JA, Ferguson JW, Bates CM, Davidson JS, Lee A, Bathgate AJ, Hayes PC, Simpson KJ. The systemic inflammatory response syndrome is predictive of renal dysfunction in patients with non-paracetamol-induced acute liver failure. Gut. 2009;58:443–9.

    Article  CAS  PubMed  Google Scholar 

  141. Jin S, Fu Q, Wuyun G, Wuyun T. Management of post-hepatectomy complications. World J Gastroenterol. 2013;19:7983–91.

    Article  PubMed Central  PubMed  Google Scholar 

  142. Gill RQ, Sterling RK. Acute liver failure. J Clin Gastroenterol. 2001;33:191–8.

    Article  CAS  PubMed  Google Scholar 

  143. Yadav K, Shrikhande S, Goel M. Post hepatectomy liver failure: concept of management. J Gastrointest Cancer. 2014;45:405–13.

    Article  PubMed  Google Scholar 

  144. Steiner C, Mitzner S. Experiences with MARS liver support therapy in liver failure: analysis of 176 patients of the International MARS Registry. Liver. 2002;22 Suppl 2:20–5.

    CAS  PubMed  Google Scholar 

  145. van de Kerkhove MP, de Jong KP, Rijken AM, de Pont AC, van Gulik TM. MARS treatment in posthepatectomy liver failure. Liver Int. 2003;23 Suppl 3:44–51.

    Article  PubMed  Google Scholar 

  146. Rittler P, Ketscher C, Inthorn D, Jauch KW, Hartl WH. Use of the molecular adsorbent recycling system in the treatment of postoperative hepatic failure and septic multiple organ dysfunction–preliminary results. Liver Int. 2004;24:136–41.

    Article  PubMed  Google Scholar 

  147. Chan SC, Sharr WW, Chan AC, Chok KS, Lo CM. Rescue Living-donor Liver Transplantation for Liver Failure Following Hepatectomy for Hepatocellular Carcinoma. Liver Cancer. 2013;2:332–7.

    Article  PubMed Central  PubMed  Google Scholar 

  148. Otsuka Y, Duffy JP, Saab S, Farmer DG, Ghobrial RM, Hiatt JR, Busuttil RW. Postresection hepatic failure: successful treatment with liver transplantation. Liver Transpl. 2007;13:672–9.

    Article  PubMed  Google Scholar 

  149. Nanashima A, Abo T, Arai J, Matsumoto H, Kudo T, Nagayasu T. Functional liver reserve parameters predictive for posthepatectomy complications. J Surg Res. 2013;185:127–35.

    Article  PubMed  Google Scholar 

  150. Kim SH, Kang DR, Lee JG, Kim do Y, Ahn SH, Han KH, Chon CY, Kim KS. Early predictor of mortality due to irreversible posthepatectomy liver failure in patients with hepatocellular carcinoma. World J Surg. 2013;37:1028–33.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Timothy M. Pawlik.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lafaro, K., Buettner, S., Maqsood, H. et al. Defining Post Hepatectomy Liver Insufficiency: Where do We stand?. J Gastrointest Surg 19, 2079–2092 (2015). https://doi.org/10.1007/s11605-015-2872-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11605-015-2872-6

Keywords

Navigation