Journal of Gastrointestinal Surgery

, Volume 21, Issue 3, pp 472–486 | Cite as

Enhanced Recovery after Surgery Programs for Liver Resection: a Meta-analysis

  • Cheng Wang
  • Guoqun Zheng
  • Wenlong Zhang
  • Fabiao Zhang
  • Shangdong Lv
  • Aidong Wang
  • Zheping FangEmail author
Original Article


Background and Aims

Due to the limited number of high-quality randomized controlled trials on enhanced recovery after surgery for hepatectomy, previous reviews have not been sufficiently comprehensive. Our objectives were to evaluate and compare the safety and efficacy of enhanced recovery after surgery programs and traditional care in patients undergoing open or laparoscopic surgery and to assess the optimized items for hepatectomy.


We searched the PubMed, Embase, and the Cochrane Library databases for all the relevant studies regardless of study design. We assessed the methodological quality of the included studies and excluded studies of poor quality. We performed a meta-analysis using RevMan 5.3 software.


In total, 19 original studies with 2575 patients, including four randomized controlled trials and 15 non-randomized controlled trials, were analyzed. The meta-analysis demonstrated that enhanced recovery after surgery programs could reduce morbidity, hospital stays and cost, blood loss, and time to bowel function recovery for both open and laparoscopic surgery without increasing mortality, readmission rate, or transfusion rate. Twelve items were essential for liver surgery.


Enhanced recovery after surgery programs for hepatectomy are feasible and efficient. Further studies should optimize perioperative outcomes for liver surgery.


Enhanced recovery after surgery Liver resection Liver surgery Hepatectomy Meta-analysis 



Our deepest gratitude goes to the authors of all the included studies and others who helped improve this paper substantially.

Author Contributions

Cheng Wang and Zheping Fang designed the study; Cheng Wang and Guoqun Zheng performed the literature search; Cheng Wang and Wenlong Zhang collected the data; Cheng Wang and Fabiao Zhang assessed the literature quality; Cheng Wang, Zheping Fang, Shangdong Lv, and Aidong Wang analyzed the data; and Cheng Wang wrote the manuscript.

Compliance with Ethical Standards

Grant Support

Our study was supported by the Science Technology Program of Zhejiang Province through the Zhejiang Provincial Health Department Project (grant no. 2015KYB434, 2017KY161), Zhejiang natural fund project of China (LY17H160069), Taizhou science and technology plan project (1602KY21, 162yw03, 14SF03).

Conflicts of Interest

The authors declare that they have no conflict of interest.


  1. 1.
    Basse L, Hjort Jakobsen D, Billesbolle P, Werner M, Kehlet H. A clinical pathway to accelerate recovery after colonic resection. Ann Surg 2000;232:51–57.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Kehlet H. Multimodal approach to control postoperative pathophysiology and rehabilitation. Br J Anaesth 1997;78:606–617.CrossRefPubMedGoogle Scholar
  3. 3.
    Kehlet H, Wilmore DW. Multimodal strategies to improve surgical outcome. Am J Surg 2002;183:630–641.CrossRefPubMedGoogle Scholar
  4. 4.
    Lassen K, Soop M, Nygren J, Cox PB, Hendry PO, Spies C, von Meyenfeldt MF, Fearon KC, Revhaug A, Norderval S, Ljungqvist O, Lobo DN, Dejong CH, Enhanced Recovery After Surgery Group. Consensus review of optimal perioperative care in colorectal surgery: Enhanced Recovery After Surgery Group (ERAS) recommendations. Arch Surg 2009;144:961–969. doi: 10.1001/archsurg.2009.170.CrossRefPubMedGoogle Scholar
  5. 5.
    Rawlinson A, Kang P, Evans J, Khanna A. A systematic review of enhanced recovery protocols in colorectal surgery. Ann R Coll Surg Engl 2011;93:583–588. doi: 10.1308/147870811X605219.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Kim JW, Kim WS, Cheong JH, Hyung WJ, Choi SH, Noh SH. Safety and efficacy of fast-track surgery in laparoscopic distal gastrectomy for gastric cancer: a randomized clinical trial. World J Surg 2012;36:2879–2887. doi: 10.1007/s00268-012-1741-7.CrossRefPubMedGoogle Scholar
  7. 7.
    Muehling B, Schelzig H, Steffen P, Meierhenrich R, Sunder-Plassmann L, Orend KH. A prospective randomized trial comparing traditional and fast-track patient care in elective open infrarenal aneurysm repair. World J Surg 2009;33:577–585. doi: 10.1007/s00268-008-9892-2.CrossRefPubMedGoogle Scholar
  8. 8.
    Jones EL, Wainwright TW, Foster JD, Smith JR, Middleton RG, Francis NK. A systematic review of patient reported outcomes and patient experience in enhanced recovery after orthopaedic surgery. Ann R Coll Surg Engl 2014;96:89–94. doi: 10.1308/003588414X13824511649571.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Arsalani-Zadeh R, ElFadl D, Yassin N, MacFie J. Evidence-based review of enhancing postoperative recovery after breast surgery. Br J Surg 2011;98:181–196. doi: 10.1002/bjs.7331.CrossRefPubMedGoogle Scholar
  10. 10.
    Kirsh EJ, Worwag EM, Sinner M, Chodak GW. Using outcome data and patient satisfaction surveys to develop policies regarding minimum length of hospitalization after radical prostatectomy. Urology 2000;56:106–107.CrossRefGoogle Scholar
  11. 11.
    Lv D, Wang X, Shi G. Perioperative enhanced recovery programmes for gynaecological cancer patients. Cochrane Database Syst Rev 2010;3:CD008239. doi: 10.1002/14651858.CD008239.pub2.Google Scholar
  12. 12.
    van den Broek MA, van Dam RM, van Breukelen GJ, Bemelmans MH, Oussoultzoglou E, Pessaux P, Dejong CH, Freemantle N, Olde Damink SW. Development of a composite endpoint for randomized controlled trials in liver surgery. Br J Surg 2011;98:1138–1145. doi: 10.1002/bjs.7503.CrossRefPubMedGoogle Scholar
  13. 13.
    Wainess RM, Cowan JA. National trends in the use and outcomes of hepatic resection. J Am Coll Surg 2004;199:31–38.PubMedGoogle Scholar
  14. 14.
    Jarnagin WR, Gonen M, Fong Y, DeMatteo RP, Ben-Porat L, Little S, Corvera C, Weber S, Blumgart LH. Improvement in perioperative outcome after hepatic resection: analysis of 1,803 consecutive cases over the past decade. Ann Surg 2002;236:397–406; discussion 406–397. doi: 10.1097/01.SLA.0000029003.66466.B3.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Melloul E, Hübner M, Scott M, Snowden C, Prentis J, Dejong CHC, Garden OJ, Farges O, Kokudo N, Vauthey JN. Guidelines for perioperative care for liver surgery: Enhanced Recovery After Surgery (ERAS) Society recommendations. World J Surg 2016;40:2425–2440.Google Scholar
  16. 16.
    Hughes MJ, McNally S, Wigmore SJ. Enhanced recovery following liver surgery: a systematic review and meta-analysis. HPB (Oxford) 2014;16:699–706. doi: 10.1111/hpb.12245.CrossRefGoogle Scholar
  17. 17.
    Coolsen MM, Wong-Lun-Hing EM, van Dam RM, van der Wilt AA, Slim K, Lassen K, Dejong CH. A systematic review of outcomes in patients undergoing liver surgery in an enhanced recovery after surgery pathways. HPB (Oxford) 2013;15:245–251. doi: 10.1111/j.1477-2574.2012.00572.x.CrossRefGoogle Scholar
  18. 18.
    Song W, Wang K, Zhang RJ, Dai QX, Zou SB. The enhanced recovery after surgery (ERAS) program in liver surgery: a meta-analysis of randomized controlled trials. Springerplus 2016;5:207. doi: 10.1186/s40064-016-1793-5. Song W and Wang K shared co-first authorship.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Ni TG, Yang HT, Zhang H, Meng HP, Li B. Enhanced recovery after surgery programs in patients undergoing hepatectomy: a meta-analysis. World J Gastroenterol 2015;21:9209–9216.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Lei Q, Wang X, Tan S, Xia X, Zheng H, Wu C. Fast-track programs versus traditional care in hepatectomy: a meta-analysis of randomized controlled trials. Dig Surg 2014;31:392–399. doi: 10.1159/000369219.CrossRefPubMedGoogle Scholar
  21. 21.
    Wu SJ, Xiong XZ, Lu J, Cheng Y, Lin YX, Zhou RX, Cheng NS. Fast-Track Programs for Liver Surgery: A Meta-Analysis. J Gastrointest Surg 2015;19:1640–1652. doi: 10.1007/s11605-015-2879-z.CrossRefPubMedGoogle Scholar
  22. 22.
    Moher D, Liberati A, Tetzlaff J, Altman DG, Prisma Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 2010;8:336–341. doi: 10.1016/j.ijsu.2010.02.007.CrossRefPubMedGoogle Scholar
  23. 23.
    Higgins JPT, Altman DG, Sterne JAC. Assessing risk of bias in included studies. In Higgins JPT, Green S, eds. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0. The Cochrane Collaboration, 2011.Google Scholar
  24. 24.
    Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M. The Newcastle Ottawa 1 Scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses. 2014.
  25. 25.
    Sun X, Ioannidis JP, Agoritsas T, Alba AC, Guyatt G. How to use a subgroup analysis: users’ guide to the medical literature. JAMA 2014;311:405–411. doi: 10.1001/jama.2013.285063.CrossRefPubMedGoogle Scholar
  26. 26.
    Furlan AD, Tomlinson G, Jadad AA, Bombardier C. Examining heterogeneity in meta-analysis: comparing results of randomized trials and nonrandomized studies of interventions for low back pain. Spine 2008;33:339–348. doi: 10.1097/BRS.0b013e31816233b5.CrossRefPubMedGoogle Scholar
  27. 27.
    Deeks JJ, Higgins JPT, Altman DG. Analyzing data and undertaking meta-analyses. In Higgins JPT, Green S, Altman DG, eds. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0. The Cochrane Collaboration, 2011.Google Scholar
  28. 28.
    Sterne JAC, Egger M, Moher D. Addressing reporting biases. In Higgins JPT, Green S, eds. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0. The Cochrane Collaboration, 2011.Google Scholar
  29. 29.
    Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 2005;5:13. doi: 10.1186/1471-2288-5-13.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    He F, Lin X, Xie F, Huang Y, Yuan R. The effect of enhanced recovery program for patients undergoing partial laparoscopic hepatectomy of liver cancer. Clin Transl Oncol 2015;17:694–701. doi: 10.1007/s12094-015-1296-9.CrossRefPubMedGoogle Scholar
  31. 31.
    Lu H, Fan Y, Zhang F, Li G, Zhang C, Lu L. Fast-track surgery improves postoperative outcomes after hepatectomy. Hepatogastroenterology 2014;61:168–172. Lu H and Fan Y shared co-first authorship.PubMedGoogle Scholar
  32. 32.
    Ni CY, Yang Y, Chang YQ, Cai H, Xu B, Yang F, Lau WY, Wang ZH, Zhou WP. 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;39:542–547. doi: 10.1016/j.ejso.2013.03.013. Ni CY and Yang Y shared co-first authorship.CrossRefPubMedGoogle Scholar
  33. 33.
    Jones C, Kelliher L, Dickinson M, Riga A, Worthington T, Scott MJ, Vandrevala T, Fry CH, Karanjia N, Quiney N. Randomized clinical trial on enhanced recovery versus standard care following open liver resection. Br J Surg 2013;100:1015–1024. doi: 10.1002/bjs.9165.CrossRefPubMedGoogle Scholar
  34. 34.
    Blind PJ, Andersson B, Tingstedt B, Bergenfeldt M, Andersson R, Lindell G, Sturesson C. Fast-track program for liver resection—factors prolonging length of stay. Hepatogastroenterology 2014;61:2340–2344.PubMedGoogle Scholar
  35. 35.
    Clark CJ, Ali SM, Zaydfudim V, Jacob AK, Nagorney DM. Safety of an Enhanced Recovery Pathway for Patients Undergoing Open Hepatic Resection. PLoS One 2016;11:e0150782. doi: 10.1371/journal.pone.0150782.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Dasari BV, Rahman R, Khan S, Bennett D, Hodson J, Isaac J, Marudanayagam R, Mirza DF, Muiesan P, Roberts KJ, Sutcliffe RP. Safety and feasibility of an enhanced recovery pathway after a liver resection: prospective cohort study. HPB (Oxford) 2015;17:700–706. doi: 10.1111/hpb.12447.CrossRefGoogle Scholar
  37. 37.
    Day RW, Cleeland CS, Wang XS, Fielder S, Calhoun J, Conrad C, Vauthey JN, Gottumukkala V, Aloia TA. Patient-reported outcomes accurately measure the value of an enhanced recovery program in liver surgery. J Am Coll Surg 2015;221:1023–1030.e1021-1022. doi: 10.1016/j.jamcollsurg.2015.09.011. Day RW, Gottumukkala V, and Aloia TA shared co-first authorship.
  38. 38.
    Joliat GR, Labgaa I, Hubner M, Blanc C, Griesser AC, Schafer M, Demartines N. Cost-benefit analysis of the implementation of an enhanced recovery program in liver surgery. World J Surg 2016;40:2441–2450. doi: 10.1007/s00268-016-3582-2.CrossRefPubMedGoogle Scholar
  39. 39.
    Kaibori M, Matsui K, Ishizaki M, Iida H, Yoshii K, Asano H, Kon M. Effects of implementing an “enhanced recovery after surgery” program on patients undergoing resection of hepatocellular carcinoma. Surg Today 2016;47:42–51. doi: 10.1007/s00595-016-1344-2.CrossRefPubMedGoogle Scholar
  40. 40.
    Labgaa I, Jarrar G, Joliat GR, Allemann P, Gander S, Blanc C, Hubner M, Demartines N. Implementation of enhanced recovery (ERAS) in colorectal surgery has a positive impact on non-ERAS liver surgery patients. World J Surg 2016;40:1082–1091. doi: 10.1007/s00268-015-3363-3. Labgaa I and Jarrar G shared co-first authorship.CrossRefPubMedGoogle Scholar
  41. 41.
    Liang X, Ying H, Wang H, Xu H, Yu H, Cai L, Wang Y, Tong Y, Ji L, Luo R, Cai XJ. Enhanced recovery program versus traditional care in laparoscopic hepatectomy. Medicine (Baltimore) 2016;95:e2835. doi: 10.1097/md.0000000000002835. Liang X and Ying H shared co-first authorship.CrossRefGoogle Scholar
  42. 42.
    Lin DX, Li X, Ye QW, Lin F, Li LL, Zhang QY. Implementation of a fast-track clinical pathway decreases postoperative length of stay and hospital charges for liver resection. Cell Biochem Biophys 2011;61:413–419. doi: 10.1007/s12013-011-9203-7.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Page AJ, Gani F, Crowley KT, Lee KH, Grant MC, Zavadsky TL, Hobson D, Wu C, Wick EC, Pawlik TM. Patient outcomes and provider perceptions following implementation of a standardized perioperative care pathway for open liver resection. Br J Surg 2016;103:564–571. doi: 10.1002/bjs.10087.CrossRefPubMedGoogle Scholar
  44. 44.
    Sanchez-Perez B, Aranda-Narvaez JM, Suarez-Munoz MA, Eladel-Delfresno M, Fernandez-Aguilar JL, Perez-Daga JA, Pulido-Roa Y, Santoyo-Santoyo J. Fast-track program in laparoscopic liver surgery: theory or fact? World J Gastrointest Surg 2012;4:246–250. doi: 10.4240/wjgs.v4.i11.246.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Savikko J, Ilmakunnas M, Makisalo H, Nordin A, Isoniemi H. Enhanced recovery protocol after liver resection. Br J Surg 2015;102:1526–1532. doi: 10.1002/bjs.9912.CrossRefPubMedGoogle Scholar
  46. 46.
    Stoot JH, van Dam RM, Busch OR, van Hillegersberg R, De Boer M, Olde Damink SWM, Bemelmans MH, Dejong CHC. The effect of a multimodal fast-track programme on outcomes in laparoscopic liver surgery: a multicentre pilot study. HPB 2009;11:140–144.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Van Dam RM, Hendry PO, Coolsen MME, Bemelmans MHA, Lassen K, Revhaug A, Fearon KCH, Garden OJ, Dejong CHC. Initial experience with a multimodal enhanced recovery programme in patients undergoing liver resection. Br J Surg 2008;95:969–975.CrossRefPubMedGoogle Scholar
  48. 48.
    Zhu L, Li J, Li XK, Feng JQ, Gao JM. Impact of a clinical pathway on hospital costs, length of stay and early outcomes after hepatectomy for hepatocellular carcinoma. Asian Pac J Cancer Prev 2014;15:5389–5393. Zhu L, Li J, Li XK and Feng JQ shared co-first authorship.CrossRefPubMedGoogle Scholar
  49. 49.
    Khuri SF, Henderson WG, DePalma RG, Mosca C, Healey NA, Kumbhani DJ, Participants in the V. A. National Surgical Quality Improvement Program. Determinants of long-term survival after major surgery and the adverse effect of postoperative complications. Ann Surg 2005;242:326–341; discussion 341–323.PubMedPubMedCentralGoogle Scholar
  50. 50.
    van Dam RM, Wong-Lun-Hing EM, Breukelen GJV, Stoot JH, Vorst JRVD, Bemelmans MH, Damink SWO, Lassen K, Dejong CH. Open versus laparoscopic left lateral hepatic sectionectomy within an enhanced recovery ERAS® programme (ORANGE II – Trial): study protocol for a randomised controlled trial. Trials 2012;13:1–11. doi: 10.1186/1745-6215-13-54.CrossRefGoogle Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2017

Authors and Affiliations

  1. 1.Department of Hepatobiliary Surgery, Taizhou Hospital of Zhejiang ProvinceWenzhou Medical UniversityLinhaiChina

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