Hepatic function assessment to predict post-hepatectomy liver failure: what can we trust? A systematic review


Post hepatectomy liver failure (PHLF) could occur even though an adequate liver volume is preserved. Liver function is not strictly related to the volume and the necessity to pre-operatively predict the future liver remnant (FLR) function is emerging, together with the wide spreading of techniques, aiming to optimize the FLR. The aim of this study was to systematically review all the available tests, to pre-operatively assess the liver function and to estimate the risk of PHLF. A systematic literature research of Medline, Embase, Scopus was performed in accordance to the preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines, to identify all the studies available for pre-operative liver function tests to assess the risk of PHLF and/or complications. From the 1122 references retrieved, 79 were included in the review. Dynamic functional tests, such as indocyanine green test (ICG), could evaluate only global liver function, with no definition of functional capacity of the remnant. Magnetic resonance imaging (MRI) with liver-specific contrast agents enables both liver function and volume evaluation; the absence of ionizing radiation showed a better patient’s compliance. Nuclear imaging studies as hepatobiliary scintigraphy (HBS) present the unique ability to allow a precise evaluation of the segmental liver function of the remnant liver. Liver volume could overestimate liver function. Several liver function tests are available to evaluate the risk of PHLF in the pre-operative setting. However, no single test alone could accurately predict PHLF. Pre-operative combination between a dynamic quantitative test, such as ICG, with MRI or HBS, should enable a more complete functional evaluation. Functional tests to predict PHLF should be chosen according to patient’s characteristics, disease, and center experience.

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

Fig. 1


  1. 1.

    Bennink RJ, Dinant S, Erdogan D, Heijnen BH, Straatsburg IH, van Vliet AK, van Gulik TM (2004) Preoperative assessment of postoperative remnant liver function using hepatobiliary scintigraphy. J Nucl Med 45(6):965–971

    PubMed  Google Scholar 

  2. 2.

    Tomassini F, D'Asseler Y, Giglio MC, Lecluyse C, Lambert B, Sainz-Barriga M, Van Dorpe J, Hoorens A, Geboes K, Troisi RI (2019) Hemodynamic changes in ALPPS influence liver regeneration and function: results from a prospective study. HPB Off J Int Hepato Pancreato Biliary Assoc 21(5):557–565. https://doi.org/10.1016/j.hpb.2018.09.005

    Article  Google Scholar 

  3. 3.

    Chapelle T, Op de Beeck B, Driessen A, Roeyen G, Bracke B, Hartman V, Huyghe I, Morrison S, Ysebaert D, Francque S (2017) Estimation of the future remnant liver function is a better tool to predict post-hepatectomy liver failure than platelet-based liver scores. Eur J Surg Oncol 43(12):2277–2284. https://doi.org/10.1016/j.ejso.2017.08.009

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Olthof PB, Coelen RJS, Bennink RJ, Heger M, Lam MF, Besselink MG, Busch OR, van Lienden KP, van Gulik TM (2017) (99m)Tc-mebrofenin hepatobiliary scintigraphy predicts liver failure following major liver resection for perihilar cholangiocarcinoma. HPB Off J Int Hepato Pancreato Biliary Assoc 19(10):850–858. https://doi.org/10.1016/j.hpb.2017.05.007

    Article  Google Scholar 

  5. 5.

    Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8(5):336–341. https://doi.org/10.1016/j.ijsu.2010.02.007

    Article  PubMed  Google Scholar 

  6. 6.

    Wagener G (2013) Assessment of hepatic function, operative candidacy, and medical management after liver resection in the patient with underlying liver disease. Semin Liver Dis 33(3):204–212. https://doi.org/10.1055/s-0033-1351777

    Article  PubMed  Google Scholar 

  7. 7.

    Mizuguchi T, Kawamoto M, Meguro M, Hui TT, Hirata K (2014) Preoperative liver function assessments to estimate the prognosis and safety of liver resections. Surg Today 44(1):1–10. https://doi.org/10.1007/s00595-013-0534-4

    Article  PubMed  Google Scholar 

  8. 8.

    Ge PL, Du SD, Mao YL (2014) Advances in preoperative assessment of liver function. Hepatobiliary Pancreat Dis Int 13(4):361–370. https://doi.org/10.1016/s1499-3872(14)60267-8

    Article  PubMed  Google Scholar 

  9. 9.

    de Graaf W, Bennink RJ, Vetelainen R, van Gulik TM (2010) Nuclear imaging techniques for the assessment of hepatic function in liver surgery and transplantation. J Nucl Med 51(5):742–752. https://doi.org/10.2967/jnumed.109.069435

    Article  PubMed  Google Scholar 

  10. 10.

    Rassam F, Olthof PB, Bennink RJ, van Gulik TM (2017) Current modalities for the assessment of future remnant liver function. Visc Med 33(6):442–448. https://doi.org/10.1159/000480385

    Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Ba-Ssalamah A, Bastati N, Wibmer A, Fragner R, Hodge JC, Trauner M, Herold CJ, Bashir MR, Van Beers BE (2017) Hepatic gadoxetic acid uptake as a measure of diffuse liver disease: Where are we? J Magn Reson Imaging 45(3):646–659. https://doi.org/10.1002/jmri.25518

    Article  PubMed  Google Scholar 

  12. 12.

    Cieslak KP, Runge JH, Heger M, Stoker J, Bennink RJ, van Gulik TM (2014) New perspectives in the assessment of future remnant liver. Dig Surg 31(4–5):255–268. https://doi.org/10.1159/000364836

    Article  PubMed  Google Scholar 

  13. 13.

    Ren Z, Xu Y, Zhu S (2012) Indocyanine green retention test avoiding liver failure after hepatectomy for hepatolithiasis. Hepatogastroenterology 59(115):782–784. https://doi.org/10.5754/hge11453

    Article  PubMed  Google Scholar 

  14. 14.

    Uchiyama K, Mori K, Tabuse K, Ueno M, Ozawa S, Nakase T, Kawai M, Tani M, Tanimura H, Yamaue H (2008) Assessment of liver function for successful hepatectomy in patients with hepatocellular carcinoma with impaired hepatic function. J Hepato-Biliary-Pancreat Surg 15(6):596–602. https://doi.org/10.1007/s00534-007-1326-2

    Article  Google Scholar 

  15. 15.

    Sugimoto H, Okochi O, Hirota M, Kanazumi N, Nomoto S, Inoue S, Takeda S, Nakao A (2006) Early detection of liver failure after hepatectomy by indocyanine green elimination rate measured by pulse dye-densitometry. J Hepato-Biliary-Pancreat Surg y 13(6):543–548. https://doi.org/10.1007/s00534-006-1114-4

    Article  Google Scholar 

  16. 16.

    Wakabayashi H, Yachida S, Maeba T, Maeta H (2002) Evaluation of liver function for the application of preoperative portal vein embolization on major hepatic resection. Hepatogastroenterology 49(46):1048–1052

    PubMed  Google Scholar 

  17. 17.

    Fan ST (2002) Methods and related drawbacks in the estimation of surgical risks in cirrhotic patients undergoing hepatectomy. Hepatogastroenterology 49(43):17–20

    PubMed  Google Scholar 

  18. 18.

    Lam CM, Fan ST, Lo CM, Wong J (1999) Major hepatectomy for hepatocellular carcinoma in patients with an unsatisfactory indocyanine green clearance test. Br J Surg 86(8):1012–1017. https://doi.org/10.1046/j.1365-2168.1999.01204.x

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Torzilli G, Makuuchi M, Inoue K, Takayama T, Sakamoto Y, Sugawara Y, Kubota K, Zucchi A (1999) No-mortality liver resection for hepatocellular carcinoma in cirrhotic and noncirrhotic patients: is there a way? A prospective analysis of our approach. Arch Surg 134(9):984–992. https://doi.org/10.1001/archsurg.134.9.984

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Lau H, Man K, Fan ST, Yu WC, Lo CM, Wong J (1997) Evaluation of preoperative hepatic function in patients with hepatocellular carcinoma undergoing hepatectomy. Br J Surg 84(9):1255–1259

    CAS  PubMed  Google Scholar 

  21. 21.

    Okamoto E, Kyo A, Yamanaka N, Tanaka N, Kuwata K (1984) Prediction of the safe limits of hepatectomy by combined volumetric and functional measurements in patients with impaired hepatic function. Surgery 95(5):586–592

    CAS  PubMed  Google Scholar 

  22. 22.

    Mizumoto R, Kawarada Y, Noguchi T (1979) Preoperative estimation of operative risk in liver surgery, with special reference to functional reserve of the remnant liver following major hepatic resection. Jpn J Surg 9(4):343–349. https://doi.org/10.1007/bf02468635

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Le Roy B, Gregoire E, Cosse C, Serji B, Golse N, Adam R, Cherqui D, Mabrut JY, Le Treut YP, Vibert E (2018) Indocyanine green retention rates at 15 min predicted hepatic decompensation in a western population. World J Surg 42(8):2570–2578. https://doi.org/10.1007/s00268-018-4464-6

    Article  PubMed  Google Scholar 

  24. 24.

    Ibis C, Albayrak D, Sahiner T, Soytas Y, Gurtekin B, Sivrikoz N (2017) Value of preoperative indocyanine green clearance test for predicting post-hepatectomy liver failure in noncirrhotic patients. Med Sci Monit 23:4973–4980. https://doi.org/10.12659/msm.907306

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Derpapas MK, Contis J, Fragulidis GP, Lykoudis PM, Polymeneas G, Ntourakis S, Voros D (2013) Correlation of the ICG test with risk factors and postoperative outcomes following hepatic resection. J Balkan Union Oncol 18(3):703–707

    CAS  Google Scholar 

  26. 26.

    Greco E, Nanji S, Bromberg IL, Shah S, Wei AC, Moulton CA, Greig PD, Gallinger S, Cleary SP (2011) Predictors of peri-operative morbidity and liver dysfunction after hepatic resection in patients with chronic liver disease. HPB 13(8):559–565. https://doi.org/10.1111/j.1477-2574.2011.00329.x

    Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Scheingraber S, Richter S, Igna D, Flesch S, Kopp B, Schilling MK (2008) Indocyanine green disappearance rate is the most useful marker for liver resection. Hepatogastroenterology 55(85):1394–1399

    CAS  PubMed  Google Scholar 

  28. 28.

    Zoedler T, Ebener C, Becker H, Roeher HD (1995) Evaluation of liver function tests to predict operative risk in liver surgery. HPB Surg 9(1):13–18. https://doi.org/10.1155/1995/47538

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. 29.

    de Liguori CN, O'Reilly DA, Dajani K, Ghaneh P, Poston GJ, Wu AV (2009) 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 35(9):957–962. https://doi.org/10.1016/j.ejso.2009.02.003

    Article  Google Scholar 

  30. 30.

    Thomas MN, Weninger E, Angele M, Bosch F, Pratschke S, Andrassy J, Rentsch M, Stangl M, Hartwig W, Werner J, Guba M (2015) Intraoperative simulation of remnant liver function during anatomic liver resection with indocyanine green clearance (LiMON) measurements. HPB 17(6):471–476. https://doi.org/10.1111/hpb.12380

    Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Weinberg L, Robinson C, Goh SK, Muralidharan V (2018) Use of indocyanine green dye clearance in a patient with liver cirrhosis undergoing hepatectomy: a clinical image. BMJ Case Rep. https://doi.org/10.1136/bcr-2018-225503

    Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Okochi O, Kaneko T, Sugimoto H, Inoue S, Takeda S, Nakao A (2002) ICG pulse spectrophotometry for perioperative liver function in hepatectomy. J Surg Res 103(1):109–113. https://doi.org/10.1006/jsre.2001.6328

    Article  PubMed  Google Scholar 

  33. 33.

    Kambakamba P, Stocker D, Reiner CS, Nguyen-Kim TD, Linecker M, Eshmuminov D, Petrowsky H, Clavien PA, Lesurtel M (2016) Liver kinetic growth rate predicts postoperative liver failure after ALPPS. HPB 18(10):800–805. https://doi.org/10.1016/j.hpb.2016.07.005

    Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Yokoyama Y, Ebata T, Igami T, Sugawara G, Mizuno T, Yamaguchi J, Nagino M (2016) The predictive value of indocyanine green clearance in future liver remnant for posthepatectomy liver failure following hepatectomy with extrahepatic bile duct resection. World J Surg 40(6):1440–1447. https://doi.org/10.1007/s00268-016-3441-1

    Article  PubMed  Google Scholar 

  35. 35.

    Miyagawa S, Makuuchi M, Kawasaki S, Kakazu T (1995) Criteria for safe hepatic resection. Am J Surg 169(6):589–594. https://doi.org/10.1016/s0002-9610(99)80227-x

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Wang YY, Zhao XH, Ma L, Ye JZ, Wu FX, Tang J, You XM, Xiang BD, Li LQ (2018) Comparison of the ability of Child–Pugh score, MELD score, and ICG-R15 to assess preoperative hepatic functional reserve in patients with hepatocellular carcinoma. J Surg Oncol 118(3):440–445. https://doi.org/10.1002/jso.25184

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Yokoyama Y, Nishio H, Ebata T, Igami T, Sugawara G, Nagino M (2010) Value of indocyanine green clearance of the future liver remnant in predicting outcome after resection for biliary cancer. Br J Surg 97(8):1260–1268. https://doi.org/10.1002/bjs.7084

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Kim HJ, Kim CY, Park EK, Hur YH, Koh YS, Kim HJ, Cho CK (2015) Volumetric analysis and indocyanine green retention rate at 15 min as predictors of post-hepatectomy liver failure. HPB 17(2):159–167. https://doi.org/10.1111/hpb.12295

    Article  PubMed  Google Scholar 

  39. 39.

    Maruyama M, Yoshizako T, Araki H, Yoshida R, Ando S, Nakamura M, Kitagaki H (2018) Future liver remnant indocyanine green plasma clearance rate as a predictor of post-hepatectomy liver failure after portal vein embolization. Cardiovasc Intervent Radiol 41(12):1877–1884. https://doi.org/10.1007/s00270-018-2065-2

    Article  PubMed  Google Scholar 

  40. 40.

    Hwang S, Ha TY, Song GW, Jung DH, Ahn CS, Moon DB, Kim KH, Lee YJ, Lee SG (2015) Quantified risk assessment for major hepatectomy via the indocyanine green clearance rate and liver volumetry combined with standard liver volume. J Gastrointest Surg 19(7):1305–1314. https://doi.org/10.1007/s11605-015-2846-8

    Article  PubMed  Google Scholar 

  41. 41.

    Yada K, Morine Y, Ishibashi H, Mori H, Shimada M (2018) Treatment strategy for successful hepatic resection of icteric liver. J Med Investig 65(1.2):37–42. https://doi.org/10.2152/jmi.65.37

    Article  Google Scholar 

  42. 42.

    Vos JJ, Wietasch JK, Absalom AR, Hendriks HG, Scheeren TW (2014) Green light for liver function monitoring using indocyanine green? An overview of current clinical applications. Anaesthesia 69(12):1364–1376. https://doi.org/10.1111/anae.12755

    CAS  Article  PubMed  Google Scholar 

  43. 43.

    Kokudo T, Hasegawa K, Amikura K, Uldry E, Shirata C, Yamaguchi T, Arita J, Kaneko J, Akamatsu N, Sakamoto Y, Takahashi A, Sakamoto H, Makuuchi M, Matsuyama Y, Demartines N, Malago M, Kokudo N, Halkic N (2016) Assessment of preoperative liver function in patients with hepatocellular carcinoma—the albumin-indocyanine green evaluation (ALICE) grade. PLoS ONE 11(7):e0159530. https://doi.org/10.1371/journal.pone.0159530

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Russolillo N, Forchino F, Conci S, Mele C, Langella S, Ruzzenente A, Scoleri I, Giuliante F, Guglielmi A, Ferrero A (2019) Validation of the albumin-indocyanine green evaluation model in patients with resected hepatocellular carcinoma and comparison with the albumin-bilirubin score. J Hepato-Biliary-Pancreat Sci 26(1):51–57. https://doi.org/10.1002/jhbp.597

    Article  Google Scholar 

  45. 45.

    Miyazaki Y, Kokudo T, Amikura K, Takahashi A, Ohkohchi N, Sakamoto H (2019) Albumin-indocyanine green evaluation grading system predicts post-hepatectomy liver failure for biliary tract cancer. Dig Surg 36(1):13–19. https://doi.org/10.1159/000486142

    CAS  Article  PubMed  Google Scholar 

  46. 46.

    Stockmann M, Lock JF, Riecke B, Heyne K, Martus P, Fricke M, Lehmann S, Niehues SM, Schwabe M, Lemke AJ, Neuhaus P (2009) Prediction of postoperative outcome after hepatectomy with a new bedside test for maximal liver function capacity. Ann Surg 250(1):119–125. https://doi.org/10.1097/SLA.0b013e3181ad85b5

    Article  PubMed  Google Scholar 

  47. 47.

    Stockmann M, Lock JF, Malinowski M, Niehues SM, Seehofer D, Neuhaus P (2010) The LiMAx test: a new liver function test for predicting postoperative outcome in liver surgery. HPB 12(2):139–146. https://doi.org/10.1111/j.1477-2574.2009.00151.x

    Article  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Lodewick TM, Alizai PH, van Dam RM, Roeth AAJ, Schmeding M, Heidenhain C, Andert A, Gassler N, Dejong CHC, Neumann UP (2017) Effect of age on liver function in patients undergoing partial hepatectomy. Dig Surg 34(3):233–240. https://doi.org/10.1159/000452494

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Lock JF, Reinhold T, Malinowski M, Pratschke J, Neuhaus P, Stockmann M (2009) The costs of postoperative liver failure and the economic impact of liver function capacity after extended liver resection—a single-center experience. Langenbeck's Arch Surg 394(6):1047–1056. https://doi.org/10.1007/s00423-009-0518-4

    CAS  Article  Google Scholar 

  50. 50.

    Malinowski M, Lock JF, Seehofer D, Gebauer B, Schulz A, Demirel L, Bednarsch J, Stary V, Neuhaus P, Stockmann M (2016) Preliminary study on liver function changes after trisectionectomy with versus without prior portal vein embolization. Surg Today 46(9):1053–1061. https://doi.org/10.1007/s00595-015-1293-1

    CAS  Article  PubMed  Google Scholar 

  51. 51.

    Morris-Stiff G, Gomez D, Prasad R (2009) Quantitative assessment of hepatic function and its relevance to the liver surgeon. J Gastrointest Surg 13(2):374–385. https://doi.org/10.1007/s11605-008-0564-1

    CAS  Article  PubMed  Google Scholar 

  52. 52.

    Garcea G, Ong SL, Maddern GJ (2009) Predicting liver failure following major hepatectomy. Dig Liver Dis 41(11):798–806. https://doi.org/10.1016/j.dld.2009.01.015

    CAS  Article  PubMed  Google Scholar 

  53. 53.

    Lorf T, Schnitzbauer AA, Schaefers SK, Scherer MN, Schlitt HJ, Oellerich M, Becker H, Obed A (2008) Prognostic value of the monoethylglycinexylidide (MEGX)-test prior to liver resection. Hepatogastroenterology 55(82–83):539–543

    CAS  PubMed  Google Scholar 

  54. 54.

    Wibmer A, Prusa AM, Nolz R, Gruenberger T, Schindl M, Ba-Ssalamah A (2013) Liver failure after major liver resection: risk assessment by using preoperative Gadoxetic acid-enhanced 3-T MR imaging. Radiology 269(3):777–786. https://doi.org/10.1148/radiol.13130210

    Article  PubMed  Google Scholar 

  55. 55.

    Sato Y, Matsushima S, Inaba Y, Sano T, Yamaura H, Kato M, Shimizu Y, Senda Y, Ishiguchi T (2015) Preoperative estimation of future remnant liver function following portal vein embolization using relative enhancement on gadoxetic acid disodium-enhanced magnetic resonance imaging. Korean J Radiol 16(3):523–530. https://doi.org/10.3348/kjr.2015.16.3.523

    Article  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Barth BK, Fischer MA, Kambakamba P, Lesurtel M, Reiner CS (2016) Liver-fat and liver-function indices derived from Gd-EOB-DTPA-enhanced liver MRI for prediction of future liver remnant growth after portal vein occlusion. Eur J Radiol 85(4):843–849. https://doi.org/10.1016/j.ejrad.2016.02.008

    Article  PubMed  Google Scholar 

  57. 57.

    Asenbaum U, Kaczirek K, Ba-Ssalamah A, Ringl H, Schwarz C, Waneck F, Fitschek F, Loewe C, Nolz R (2018) Post-hepatectomy liver failure after major hepatic surgery: not only size matters. Eur Radiol 28(11):4748–4756. https://doi.org/10.1007/s00330-018-5487-y

    Article  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Costa AF, Tremblay St-Germain A, Abdolell M, Smoot RL, Cleary S, Jhaveri KS (2017) Can contrast-enhanced MRI with gadoxetic acid predict liver failure and other complications after major hepatic resection? Clin Radiol 72(7):598–605. https://doi.org/10.1016/j.crad.2017.02.004

    CAS  Article  PubMed  Google Scholar 

  59. 59.

    Cho SH, Kang UR, Kim JD, Han YS, Choi DL (2011) The value of gadoxetate disodium-enhanced MR imaging for predicting posthepatectomy liver failure after major hepatic resection: a preliminary study. Eur J Radiol 80(2):e195–200. https://doi.org/10.1016/j.ejrad.2011.08.008

    Article  PubMed  Google Scholar 

  60. 60.

    Kim DK, Choi JI, Choi MH, Park MY, Lee YJ, Rha SE, Jung SE (2018) Prediction of posthepatectomy liver failure: MRI with hepatocyte-specific contrast agent versus indocyanine green clearance test. AJR Am J Roentgenol 211(3):580–587. https://doi.org/10.2214/AJR.17.19206

    Article  PubMed  Google Scholar 

  61. 61.

    Yoon JH, Choi JI, Jeong YY, Schenk A, Chen L, Laue H, Kim SY, Lee JM (2016) Pre-treatment estimation of future remnant liver function using gadoxetic acid MRI in patients with HCC. J Hepatol 65(6):1155–1162. https://doi.org/10.1016/j.jhep.2016.07.024

    CAS  Article  PubMed  Google Scholar 

  62. 62.

    Hwang EH, Taki J, Shuke N, Nakajima K, Kinuya S, Konishi S, Michigishi T, Aburano T, Tonami N (1999) Preoperative assessment of residual hepatic functional reserve using 99mTc-DTPA-galactosyl-human serum albumin dynamic SPECT. J Nucl Med 40(10):1644–1651

    CAS  PubMed  Google Scholar 

  63. 63.

    Tanoue Y, Nanashima A, Yano K, Fujii Y, Hiyoshi M, Imamura N, Hamada T, Ikenoue M, Wada T, Mizutani Y, Hirai T (2019) Significance of the preoperative regional maximal removal rate of technetium-99m-galactosyl human serum albumin in the future remnant liver: a sequential study of regional maximal removal rate of technetium-99m-galactosyl human serum albumin in the whole liver. Nucl Med Commun 40(2):145–152. https://doi.org/10.1097/MNM.0000000000000950

    Article  PubMed  Google Scholar 

  64. 64.

    Nanashima A, Tobinaga S, Abo T, Nonaka T, Takeshita H, Hidaka S, Sawai T, Nagayasu T (2010) Reducing the incidence of post-hepatectomy hepatic complications by preoperatively applying parameters predictive of liver function. J Hepato-Biliary-Pancreat Sci 17(6):871–878. https://doi.org/10.1007/s00534-010-0281-5

    Article  Google Scholar 

  65. 65.

    Kaibori M, Ha-Kawa SK, Ishizaki M, Matsui K, Saito T, Kwon AH, Kamiyama Y (2008) HA/GSA-Rmax ratio as a predictor of postoperative liver failure. World J Surg 32(11):2410–2418. https://doi.org/10.1007/s00268-008-9725-3

    Article  PubMed  Google Scholar 

  66. 66.

    Kokudo N, Vera DR, Tada K, Koizumi M, Seki M, Matsubara T, Ohta H, Yamaguchi T, Takahashi T, Nakajima T, Muto T (2002) Predictors of successful hepatic resection: prognostic usefulness of hepatic asialoglycoprotein receptor analysis. World J Surg 26(11):1342–1347. https://doi.org/10.1007/s00268-002-6262-3

    Article  PubMed  Google Scholar 

  67. 67.

    Mizutani Y, Hirai T, Nagamachi S, Nanashima A, Yano K, Kondo K, Hiyoshi M, Imamura N, Terada T (2018) Prediction of posthepatectomy liver failure proposed by the international study group of liver surgery: residual liver function estimation with 99mTc-galactosyl human serum albumin scintigraphy. Clin Nucl Med 43(2):77–81. https://doi.org/10.1097/RLU.0000000000001913

    Article  PubMed  Google Scholar 

  68. 68.

    Yoshida M, Shiraishi S, Sakamoto F, Beppu T, Utsunomiya D, Okabe H, Tomiguchi S, Baba H, Yamashita Y (2014) Assessment of hepatic functional regeneration after hepatectomy using (99m)Tc-GSA SPECT/CT fused imaging. Ann Nucl Med 28(8):780–788. https://doi.org/10.1007/s12149-014-0872-3

    CAS  Article  PubMed  Google Scholar 

  69. 69.

    Mao Y, Du S, Ba J, Li F, Yang H, Lu X, Sang X, Li S, Che L, Tong J, Xu Y, Xu H, Zhao H, Chi T, Liu F, Du Y, Zhang X, Wang X, Dong J, Zhong S, Huang J, Yu Y, Wang J (2015) Using dynamic 99mT c-GSA SPECT/CT fusion images for hepatectomy planning and postoperative liver failure prediction. Ann Surg Oncol 22(4):1301–1307. https://doi.org/10.1245/s10434-014-4117-4

    Article  PubMed  Google Scholar 

  70. 70.

    Hayashi H, Beppu T, Okabe H, Kuroki H, Nakagawa S, Imai K, Nitta H, Chikamoto A, Ishiko T, Baba H (2015) Functional assessment versus conventional volumetric assessment in the prediction of operative outcomes after major hepatectomy. Surgery 157(1):20–26. https://doi.org/10.1016/j.surg.2014.06.013

    Article  PubMed  Google Scholar 

  71. 71.

    Tatsumi H, Masuda Y, Imaizumi H, Yoshida S, Goto K, Yama N, Mizuguchi T, Hirata K (2013) Asialoglycoprotein receptor scintigraphy with 99mTc-galactosyl human serum albumin (99mTc-GSA) as an early predictor of survival in acute liver failure. Anaesth Intensive Care 41(4):523–528. https://doi.org/10.1177/0310057X1304100414

    CAS  Article  PubMed  Google Scholar 

  72. 72.

    Nanashima A, Abo T, Arai J, Matsumoto H, Kudo T, Nagayasu T (2013) Functional liver reserve parameters predictive for posthepatectomy complications. J Surg Res 185(1):127–135. https://doi.org/10.1016/j.jss.2013.05.021

    Article  PubMed  Google Scholar 

  73. 73.

    Sumiyoshi T, Shima Y, Okabayashi T, Kozuki A, Hata Y, Noda Y, Kouno M, Miyagawa K, Tokorodani R, Saisaka Y, Tokumaru T, Nakamura T, Morita S (2016) Liver function assessment using 99mTc-GSA single-photon emission computed tomography (SPECT)/CT fusion imaging in hilar bile duct cancer: a retrospective study. Surgery 160(1):118–126. https://doi.org/10.1016/j.surg.2016.02.009

    Article  PubMed  Google Scholar 

  74. 74.

    Okabayashi T, Shima Y, Morita S, Shimada Y, Sumiyoshi T, Sui K, Iwata J, Iiyama T (2017) Liver function assessment using technetium 99m-galactosyl single-photon emission computed tomography/CT fusion imaging: a prospective trial. J Am Coll Surg 225(6):789–797. https://doi.org/10.1016/j.jamcollsurg.2017.08.021

    Article  PubMed  Google Scholar 

  75. 75.

    Sumiyoshi T, Okabayashi T, Negoro Y, Hata Y, Noda Y, Sui K, Iwata J, Matsumoto M (2018) (99m)Tc-GSA SPECT/CT fusion imaging for hepatectomy candidates with extremely deteriorated ICG value. Jpn J Radiol 36(9):537–543. https://doi.org/10.1007/s11604-018-0753-0

    Article  PubMed  Google Scholar 

  76. 76.

    Yoshida M, Beppu T, Shiraishi S, Tsuda N, Sakamoto F, Kuramoto K, Okabe H, Nitta H, Imai K, Tomiguchi S, Baba H, Yamashita Y (2018) Liver function in areas of hepatic venous congestion after hepatectomy for liver cancer: (99m)Tc-GSA SPECT/CT fused imaging study. Anticancer Res 38(5):3089–3095. https://doi.org/10.21873/anticanres.12567

    CAS  Article  PubMed  Google Scholar 

  77. 77.

    Nakamura I, Iimuro Y, Hai S, Kondo Y, Hatano E, Fujimoto J (2018) Impaired value of 99m Tc-GSA scintigraphy as an independent risk factor for posthepatectomy liver failure in patients with hepatocellular carcinoma. Eur Surg Res 59(1–2):12–22. https://doi.org/10.1159/000484044

    CAS  Article  PubMed  Google Scholar 

  78. 78.

    Yumoto Y, Yagi T, Sato S, Nouso K, Kobayashi Y, Ohmoto M, Yumoto E, Nagaya I, Nakatsukasa H (2010) Preoperative estimation of remnant hepatic function using fusion images obtained by (99m)Tc-labelled galactosyl-human serum albumin liver scintigraphy and computed tomography. Br J Surg 97(6):934–944. https://doi.org/10.1002/bjs.7025

    CAS  Article  PubMed  Google Scholar 

  79. 79.

    Chiba N, Yokozuka K, Ochiai S, Gunji T, Okihara M, Sano T, Tomita K, Tsutsui R, Kawachi S (2018) The diagnostic value of 99m-Tc GSA scintigraphy for liver function and remnant liver volume in hepatic surgery: a retrospective observational cohort study in 27 patients. Patient Saf Surg 12:15. https://doi.org/10.1186/s13037-018-0161-5

    Article  PubMed  PubMed Central  Google Scholar 

  80. 80.

    Nishiyama Y, Yamamoto Y, Hino I, Satoh K, Wakabayashi H, Ohkawa M (2003) 99mTc galactosyl human serum albumin liver dynamic SPET for pre-operative assessment of hepatectomy in relation to percutaneous transhepatic portal embolization. Nucl Med Commun 24(7):809–817. https://doi.org/10.1097/00006231-200307000-00011

    CAS  Article  PubMed  Google Scholar 

  81. 81.

    Yano K, Nanashima A, Fujii Y, Hiyoshi M, Imamura N, Hamada T, Tsuchimochi Y, Wada T, Mizutani Y, Hirai T (2017) Preoperative regional maximal removal rate of technetium-99m-galactosyl human serum albumin is correlated with liver functional parameters, but did not predict postoperative morbidity. Nucl Med Commun 38(8):701–707. https://doi.org/10.1097/MNM.0000000000000702

    CAS  Article  PubMed  Google Scholar 

  82. 82.

    Kwon AH, Ha-Kawa SK, Uetsuji S, Inoue T, Matsui Y, Kamiyama Y (1997) Preoperative determination of the surgical procedure for hepatectomy using technetium-99m-galactosyl human serum albumin (99mTc-GSA) liver scintigraphy. Hepatology 25(2):426–429. https://doi.org/10.1002/hep.510250228

    CAS  Article  PubMed  Google Scholar 

  83. 83.

    Kwon AH, Matsui Y, Kaibori M, Ha-Kawa SK (2006) Preoperative regional maximal removal rate of technetium-99m-galactosyl human serum albumin (GSA-Rmax) is useful for judging the safety of hepatic resection. Surgery 140(3):379–386. https://doi.org/10.1016/j.surg.2006.02.011

    Article  PubMed  Google Scholar 

  84. 84.

    Kobayashi K, Hattori N, Manabe O, Hirata K, Magota K, Shimamura T, Tamaki N (2015) Postoperative assessment of hepatic asialoglycoprotein receptor function with Tc-99m GSA: the safety margin of resection size in living donor liver transplantation. Ann Transplant 20:51–58. https://doi.org/10.12659/AOT.892490

    CAS  Article  PubMed  Google Scholar 

  85. 85.

    Geisel D, Ludemann L, Froling V, Malinowski M, Stockmann M, Baron A, Gebauer B, Seehofer D, Prasad V, Denecke T (2015) Imaging-based evaluation of liver function: comparison of (9)(9)mTc-mebrofenin hepatobiliary scintigraphy and Gd-EOB-DTPA-enhanced MRI. Eur Radiol 25(5):1384–1391. https://doi.org/10.1007/s00330-014-3536-8

    Article  PubMed  Google Scholar 

  86. 86.

    de Graaf W, van Lienden KP, Dinant S, Roelofs JJ, Busch OR, Gouma DJ, Bennink RJ, van Gulik TM (2010) Assessment of future remnant liver function using hepatobiliary scintigraphy in patients undergoing major liver resection. J Gastrointest Surg 14(2):369–378. https://doi.org/10.1007/s11605-009-1085-2

    Article  PubMed  Google Scholar 

  87. 87.

    Rassam F, Olthof PB, Richardson H, van Gulik TM, Bennink RJ (2019) Practical guidelines for the use of technetium-99m mebrofenin hepatobiliary scintigraphy in the quantitative assessment of liver function. Nucl Med Commun 40(4):297–307. https://doi.org/10.1097/MNM.0000000000000973

    Article  PubMed  Google Scholar 

  88. 88.

    Hoekstra LT, de Graaf W, Nibourg GA, Heger M, Bennink RJ, Stieger B, van Gulik TM (2013) Physiological and biochemical basis of clinical liver function tests: a review. Ann Surg 257(1):27–36. https://doi.org/10.1097/SLA.0b013e31825d5d47

    Article  PubMed  Google Scholar 

  89. 89.

    Tomassini F, D'Asseler Y, Linecker M, Giglio MC, Castro-Benitez C, Truant S, Axelsson R, Olthof PB, Montalti R, Serenari M, Chapelle T, Lucidi V, Sparrelid E, Adam R, Van Gulik T, Pruvot FR, Clavien PA, Bruzzese D, Geboes K, Troisi RI (2020) Hepatobiliary scintigraphy and kinetic growth rate predict liver failure after ALPPS: a multi-institutional study. HPB. https://doi.org/10.1016/j.hpb.2020.01.010

    Article  PubMed  Google Scholar 

  90. 90.

    Cieslak KP, Bennink RJ, de Graaf W, van Lienden KP, Besselink MG, Busch OR, Gouma DJ, van Gulik TM (2016) Measurement of liver function using hepatobiliary scintigraphy improves risk assessment in patients undergoing major liver resection. HPB 18(9):773–780. https://doi.org/10.1016/j.hpb.2016.06.006

    Article  PubMed  PubMed Central  Google Scholar 

  91. 91.

    Chapelle T, Op De Beeck B, Huyghe I, Francque S, Driessen A, Roeyen G, Ysebaert D, De Greef K (2016) Future remnant liver function estimated by combining liver volumetry on magnetic resonance imaging with total liver function on (99m)Tc-mebrofenin hepatobiliary scintigraphy: can this tool predict post-hepatectomy liver failure? HPB 18(6):494–503. https://doi.org/10.1016/j.hpb.2015.08.002

    Article  PubMed  PubMed Central  Google Scholar 

  92. 92.

    Chapelle T, Op de Beeck B, Roeyen G, Bracke B, Hartman V, De Greef K, Huyghe I, Van der Zijden T, Morrison S, Francque S, Ysebaert D (2017) Measuring future liver remnant function prior to hepatectomy may guide the indication for portal vein occlusion and avoid posthepatectomy liver failure: a prospective interventional study. HPB 19(2):108–117. https://doi.org/10.1016/j.hpb.2016.11.005

    Article  PubMed  Google Scholar 

  93. 93.

    Olthof PB, Tomassini F, Huespe PE, Truant S, Pruvot FR, Troisi RI, Castro C, Schadde E, Axelsson R, Sparrelid E, Bennink RJ, Adam R, van Gulik TM, de Santibanes E (2017) Hepatobiliary scintigraphy to evaluate liver function in associating liver partition and portal vein ligation for staged hepatectomy: Liver volume overestimates liver function. Surgery 162(4):775–783. https://doi.org/10.1016/j.surg.2017.05.022

    Article  PubMed  Google Scholar 

  94. 94.

    Sparrelid E, Jonas E, Tzortzakakis A, Dahlen U, Murquist G, Brismar T, Axelsson R, Isaksson B (2017) Dynamic evaluation of liver volume and function in associating liver partition and portal vein ligation for staged hepatectomy. J Gastrointest Surg 21(6):967–974. https://doi.org/10.1007/s11605-017-3389-y

    Article  PubMed  PubMed Central  Google Scholar 

  95. 95.

    Truant S, Baillet C, Deshorgue AC, El Amrani M, Huglo D, Pruvot FR (2017) Contribution of hepatobiliary scintigraphy in assessing ALPPS most suited timing. Updates Surg 69(3):411–419. https://doi.org/10.1007/s13304-017-0481-5

    Article  PubMed  Google Scholar 

  96. 96.

    de Graaf W, van Lienden KP, van den Esschert JW, Bennink RJ, van Gulik TM (2011) Increase in future remnant liver function after preoperative portal vein embolization. Br J Surg 98(6):825–834. https://doi.org/10.1002/bjs.7456

    Article  PubMed  Google Scholar 

  97. 97.

    Truant S, Baillet C, Fulbert M, Olivier A, Sergent G, Turpin A, Boleslawski E, El Amrani M, Huglo D, Pruvot FR (2019) Asymmetric kinetics of volume and function of the remnant liver after major hepatectomy as a key for postoperative outcome—a case-matched study. HPB. https://doi.org/10.1016/j.hpb.2019.10.008

    Article  PubMed  Google Scholar 

  98. 98.

    Cieslak KP, Huisman F, Bais T, Bennink RJ, van Lienden KP, Verheij J, Besselink MG, Busch ORC, van Gulik TM (2017) Future remnant liver function as predictive factor for the hypertrophy response after portal vein embolization. Surgery 162(1):37–47. https://doi.org/10.1016/j.surg.2016.12.031

    Article  PubMed  Google Scholar 

  99. 99.

    Serenari M, Pettinato C, Bonatti C, Zanoni L, Odaldi F, Cucchetti A, Ravaioli M, Fanti S, Pinna AD, Cescon M (2019) Hepatobiliary scintigraphy in the preoperative evaluation of potential living liver donors. Transpl Proc 51(1):167–170. https://doi.org/10.1016/j.transproceed.2018.04.087

    CAS  Article  Google Scholar 

  100. 100.

    Makuuchi M, Hasegawa H, Yamazaki S (1986) Indication for hepatectomy in patients with hepatocellular carcinoma and cirrhosis. Shindan Chiryo 74:1225–1230

    Google Scholar 

  101. 101.

    Takasaki K (1986) Selection of operative procedure for primary hepatocellular carcinoma, complicated with live cirrhosis—criteria on control of volume in hepatic resection in consideration of security radicality and new deloped anatomically systemized hepatic resection. Jpn J Gastroenterol Surg 19:1881–1889

    Article  Google Scholar 

  102. 102.

    Narasaki H, Noji T, Wada H, Ebihara Y, Tsuchikawa T, Okamura K, Tanaka E, Shichinohe T, Hirano S (2017) Intraoperative real-time assessment of liver function with near-infrared fluorescence imaging. Eur Surg Res 58(5–6):235–245. https://doi.org/10.1159/000477347

    CAS  Article  PubMed  Google Scholar 

Download references


The authors received no funding for this research.

Author information



Corresponding author

Correspondence to Roberto I. Troisi.

Ethics declarations

Conflict of interest

The authors declare no competing financial interest.

Research involving human participants and/or animals

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

For this type of study formal consent is not required.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tomassini, F., Giglio, M.C., De Simone, G. et al. Hepatic function assessment to predict post-hepatectomy liver failure: what can we trust? A systematic review. Updates Surg 72, 925–938 (2020). https://doi.org/10.1007/s13304-020-00859-7

Download citation


  • Hepatic function
  • Liver resection
  • Liver surgery
  • Hepatectomy
  • Post-hepatectomy liver failure