Enhanced Recovery After Surgery Program for Patients Undergoing Resection of Hepatocellular Carcinoma

  • Masaki KaiboriEmail author
  • Kosuke Matsui
  • Morihiko Ishizaki
  • Kentaro Inoue
  • Kengo Yoshii
  • Masanori Kon


A recent study at our center analyzed whether an enhanced recovery after surgery (ERAS) program for patients undergoing potentially curative liver resection for hepatocellular carcinoma (HCC) influenced the feasibility, safety, and effectiveness of surgery. Clinicopathologic factors, surgical factors, and outcomes were compared in patients who underwent extended hepatectomy (resection of more than two sections) for HCC before and after the introduction of the ERAS program. Operating time and postoperative hospital stay were significantly shorter, and total volume infused during surgery significantly lower, for the ERAS than for the control group. Although retention of abdominal drainage was significantly less frequent in the ERAS group, the frequency of abdominal paracentesis in patients without intraoperative abdominal drainage was higher in this group. Oral dietary intake and ability to walk stably occurred significantly earlier in the ERAS group. Postoperative serum concentrations of albumin and cholinesterase were significantly higher in the ERAS than in the control group. These findings showed that the ERAS program for patients with mild to moderate liver dysfunction undergoing extended liver resection for HCC was feasible and effective. It allowed earlier oral dietary intake, promoted faster postoperative recovery, and reduced overall hospital stay.


Hepatectomy Liver cancer Enhanced recovery after surgery 


  1. 1.
    Adamina M, Kehlet H, Tomlinson GA, Senagore AJ, Delaney CP. Enhanced recovery pathways optimize health outcomes and resource utilization: a meta-analysis of randomized controlled trials in colorectal surgery. Surgery. 2011;149:830–40.CrossRefPubMedGoogle Scholar
  2. 2.
    Lassen K, Soop M, Nygren J, Cox PB, Hendry PO, Spies C, et al. Consensus review of optimal perioperative care in colorectal surgery: Enhanced Recovery After Surgery (ERAS) Group recommendations. Arch Surg. 2009;144:961–9.CrossRefPubMedGoogle Scholar
  3. 3.
    Leibman BD, Dillioglugil O, Abbas F, Tanli S, Kattan MW, Scardino PT. Impact of a clinical pathway for radical retropublic prostatectomy. Urology. 1998;52:94–9.CrossRefPubMedGoogle Scholar
  4. 4.
    Niino T, Hata M, Sezai A, Yoshitake I, Unosawa S, Shimura K, et al. Optimal clinical pathway for the patient with type B acute aortic dissection. Circ J. 2009;73:264–8.CrossRefPubMedGoogle Scholar
  5. 5.
    Spanjersberg WR, Reurings J, Keus F, van Laarhoven CJ. Fast track surgery versus conventional recovery strategies for colorectal surgery. Cochrane Database Syst Rev. 2011;2:CD007635. Scholar
  6. 6.
    Hall TC, Dennison AR, Biku DK, Metcalfe MS, Garcea G. Enhanced recovery programmes in hepatobiliary and pancreatic surgery: a systematic review. Ann R Coll Surg Engl. 2012;94:318–26.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Page AJ, Ejaz A, Spolverato G, Zavadsky T, Grant MC, Galante DJ, et al. Enhanced recovery after surgery protocols for open hepatectomy: physiology, immunomodulation, and implementation. J Gastrointest Surg. 2015;19:387–99.CrossRefPubMedGoogle Scholar
  8. 8.
    Jones C, Kelliher L, Dickinson M, Riga A, Worthington T, Scott MJ, et al. Randomized clinical trial on enhanced recovery versus standard care following open liver resection. Br J Surg. 2013;100:1015–24.CrossRefPubMedGoogle Scholar
  9. 9.
    Ni CY, Yang Y, Chang YQ, Cai H, Xu B, Yang F, et al. Fast-track surgery improves postoperative recovery in patients undergoing partial hepatectomy for primary liver cancer: a prospective randomized controlled trial. Eur J Surg Oncol. 2013;39:542–7.CrossRefPubMedGoogle Scholar
  10. 10.
    Bosch X, Ribes J, Borras J. Epidemiology of primary liver cancer. Semin Liver Dis. 1999;19:271–85.CrossRefPubMedGoogle Scholar
  11. 11.
    Taylor-Robinson SD, Foster GR, Arora S, Hargreaves S, Thomas HC. Increase in primary liver cancer in the UK 1979-94. Lancet. 1997;350:1142–3.CrossRefPubMedGoogle Scholar
  12. 12.
    HB EI-S, Mason AC. Rising incidence of hepatocellular carcinoma in the United States. N Engl J Med. 1999;340:745–50.CrossRefGoogle Scholar
  13. 13.
    Nanashima A, Nagayasu T. Development and clinical usefulness of the liver hanging maneuver in various anatomical hepatectomy procedures. Surg Today. 2016;46:398–404.CrossRefPubMedGoogle Scholar
  14. 14.
    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.CrossRefPubMedGoogle Scholar
  15. 15.
    Nadig DE, Wada TP, Fairchild RB, Virgo KS, Johnson FE. Major hepatic resection. Arch Surg. 1997;132:115–9.CrossRefPubMedGoogle Scholar
  16. 16.
    Yeh CN, Chen MF, Lee WC, Jeng LB. Prognostic factors of hepatic resection for hepatocellular carcinoma with cirrhosis: univariate and multivariate analysis. J Surg Oncol. 2002;81:195–202.CrossRefPubMedGoogle Scholar
  17. 17.
    Benzoni E, Cojutti A, Lorenzin D, Adani GL, Baccarani U, Favero A, et al. Liver resective surgery: a multivariate analysis of postoperative outcome and complication. Langenbeck’s Arch Surg. 2007;392:45–54.CrossRefGoogle Scholar
  18. 18.
    Chiappa A, Zbar AP, Audisio RA, Leone BE, Biella F, Staudacher C. Factors affecting survival and long-term outcome in the cirrhotic patient undergoing hepatic resection for hepatocellular carcinoma. Eur J Surg Oncol. 2000;26:387–92.CrossRefPubMedGoogle Scholar
  19. 19.
    Farges O, Malassagne B, Flejou JF, Balzan S, Sauvanet A, Belghiti J. Risk of major liver resection in patients with underlying chronic liver disease: a reappraisal. Ann Surg. 1999;229:210–5.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Yamanaka N, Takata M, Tanaka T, Yamanaka J, Yasui C, Ando T, et al. Evolution of and obstacles in surgical treatment for hepatocellular carcinoma over the last 25 years: differences over four treatment eras. J Gastroenterol. 2000;35:613–21.CrossRefPubMedGoogle Scholar
  21. 21.
    Makuuchi M. Remodeling the surgical approach to hepatocellular carcinoma. Hepato-Gastroenterology. 2002;49:36–40.PubMedGoogle Scholar
  22. 22.
    Taketomi A, Kitagawa D, Itoh S, Harimoto N, Yamashita Y, Gion T, et al. Trends in morbidity and mortality after hepatic resection for hepatocellular carcinoma: an institute’s experience with 625 patients. J Am Coll Surg. 2007;204:580–7.CrossRefPubMedGoogle Scholar
  23. 23.
    Strasberg SM, Belghiti J, Clavn P-A. The Brisbane 2000 terminology of liver anatomy and resection. Terminology Committee of the International Hepato-Pancreato-Biliary Association. HPB. 2000;2:333–9.CrossRefGoogle Scholar
  24. 24.
    Couinaud C, editor. Le Foie: Etudes Anatomiques et Chirurgicales. Paris: Masson; 1957.Google Scholar
  25. 25.
    Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250:187–96.CrossRefPubMedGoogle Scholar
  26. 26.
    Katayama H, Kurokawa Y, Nakamura K, Ito H, Kanemitsu Y, Masuda N, et al. Extended Clavien-Dindo classification of surgical complications: Japan Clinical Oncology Group postoperative complications criteria. See comment in PubMed Commons below Surgery today Online First. 2015.
  27. 27.
    Fearon KC, Ljungqvist O, Von Meyenfeldt M, Revhaug A, Dejong CH, Lassen K, et al. Enhanced recovery after surgery: a consensus review of clinical care for patients undergoing colonic resection. Clin Nutr. 2005;24:466–77.CrossRefPubMedGoogle Scholar
  28. 28.
    Beaver WL, Wasserman K, Whipp BJ. Bicarbonate buffering of lactic acid generated during exercise. J Appl Physiol. 1986;60:472–8.CrossRefPubMedGoogle Scholar
  29. 29.
    Whipp BJ, Wasserman K. Oxygen uptake kinetics for various intensities of constant-load work. J Appl Physiol. 1972;33:351–6.CrossRefPubMedGoogle Scholar
  30. 30.
    Wasserman K, Hansen JE, Sue DY. Principles of exercise testing and interpretation. In: Wasserman K, Hansen JE, Sue DY, Whipp BJ, editors. Measurement of the physiological response to exercise. Philadelphia: Lea and Febiger; 1987. p. 27–46.Google Scholar
  31. 31.
    Snowden CP, Prentis JM, Anderson HL, et al. Submaximal cardiopulmonary exercise testing predicts complications and hospital length of stay in patients undergoing major elective surgery. Ann Surg. 2010;251:535–41.CrossRefPubMedGoogle Scholar
  32. 32.
    Kaibori M, Ishizaki M, Matsui K, Nakatake R, Yoshiuchi S, Kimura Y, et al. Perioperative exercise for chronic liver injury patients with hepatocellular carcinoma undergoing hepatectomy. Am J Surg. 2013;206:202–9.CrossRefPubMedGoogle Scholar
  33. 33.
    Lewis SJ, Egger M, Sylvester PA, Thomas S. Early enteral feeding versus ‘nil by mouth’ after gastrointestinal surgery: systematic review and meta-analysis of controlled trials. BMJ. 2001;323:773–6.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Lobo DN, Bostock KA, Neal KR, Perkins AC, Rowlands BJ, Allison SP. Effect of salt and water balance on recovery of gastrointestinal function after elective colonic resection: a randomised controlled trial. Lancet. 2002;359:1812–8.CrossRefPubMedGoogle Scholar
  35. 35.
    Kehlet H, Wilmpore DW. Multimodal strategies to improve surgical outcome. Am J Surg. 2002;183:630–41.CrossRefPubMedGoogle Scholar
  36. 36.
    Kaibori M, Ishizaki M, Matsui K, Kwon AH. Intraoperative indocyanine green fluorescent imaging for prevention of bile leakage after hepatic resection. Surgery. 2011;150:91–8.CrossRefPubMedGoogle Scholar
  37. 37.
    Kaibori M, Matsui K, Ishizaki M, Iida H, Kwon AH. In: Kusano M, Kokudo N, Toi M, Kaibori M, editors. ICG fluorescence imaging and navigation surgery. Tokyo: Springer; 2015. p. 381–388. Chap. 35.Google Scholar
  38. 38.
    Kenjo A, Miyata H, Gotoh M, Kitagawa Y, Shimada M, Baba H, et al. Risk stratification of 7,732 hepatectomy cases in 2011 from the national clinical database for Japan. J Am Coll Surg. 2014;218:412–22.CrossRefPubMedGoogle Scholar
  39. 39.
    Fong Y, Brennan MF, Brown K, Heffernan N, Blumgart LH. Drainage is unnecessary after elective liver resection. Am J Surg. 1996;171:158–62.CrossRefPubMedGoogle Scholar
  40. 40.
    Petrowsky H, Demartines N, Rousson V, Clavien PA. Evidence-based value of prophylactic drainage in gastrointestinal surgery: a systematic review and meta-analyses. Ann Surg. 2004;240:1074–84.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Belghiti J, Kabbej M, Sauvanet A, Vilgrain V, Panis Y, Fekete F. Drainage after elective hepatic resection. A randomized trial. Ann Surg. 1993;218:748–53.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Burt BM, Brown K, Jarnajin W, DeMatteo R, Blumgart LH, Fong Y. An audit of results of a no-drainage practice policy after hepatectomy. Am J Surg. 2002;184:441–5.CrossRefPubMedGoogle Scholar
  43. 43.
    Liu CL, Fan ST, Lo CM, Wong Y, Ng IO, Lam CM, et al. Abdominal drainage after hepatic resection is contraindicated in patients with chronic liver diseases. Ann Surg. 2004;239:194–201.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Masaki Kaibori
    • 1
    • 2
    Email author
  • Kosuke Matsui
    • 1
  • Morihiko Ishizaki
    • 1
  • Kentaro Inoue
    • 1
  • Kengo Yoshii
    • 3
  • Masanori Kon
    • 1
  1. 1.Department of SurgeryHirakata Hospital, Kansai Medical UniversityOsakaJapan
  2. 2.Next-generation Minimally Invasive SurgeryKansai Medical UniversityOsakaJapan
  3. 3.Department of Medical StatisticsKyoto Prefectural University of MedicineKyotoJapan

Personalised recommendations