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A systematic review and meta-analysis comparing the short- and long-term outcomes for laparoscopic and open liver resections for liver metastases from colorectal cancer

  • Ruben CiriaEmail author
  • Sira Ocaña
  • Irene Gomez-Luque
  • Federica Cipriani
  • Mark Halls
  • Åsmund Avdem Fretland
  • Yukihiro Okuda
  • Somaiah Aroori
  • Javier Briceño
  • Luca Aldrighetti
  • Bjorn Edwin
  • Mohammed Abu HilalEmail author
Article
  • 16 Downloads

Abstract

Background

The laparoscopic approach to liver resection has experienced exponential growth in recent years. However, evidence-based guidelines are needed for its safe future progression. The main aim of our study was to perform a systematic review and meta-analysis comparing the short- and long-term outcomes of laparoscopic and open liver resections for colorectal liver metastases (CRLM).

Methods

To identify all the comparative manuscripts between laparoscopic and open liver resections for CRLM, all published English language studies with more than ten cases were screened. In addition to the primary meta-analysis, 3 specific subgroup analyses were performed on patients undergoing minor-only, major-only and synchronous resections. The quality of the studies was assessed using the Scottish Intercollegiate Guidelines Network (SIGN) methodology and Newcastle–Ottawa Score.

Results

From the initial 194 manuscripts identified, 21 were meta-analysed, including results from the first randomized trial comparing open and laparoscopic resections of CRLM. Five of these were specific to patients undergoing a synchronous resection (399 cases), while six focused on minor (3 series including 226 cases) and major (3 series including 135 cases) resections, respectively. Thirteen manuscripts compared 2543 cases but could not be assigned to any of the above sub-analyses, so were analysed independently. The majority of short-term outcomes were favourable to the laparoscopic approach with equivalent rates of negative resection margins. No differences were observed between the approaches in overall or disease-free survival at 1, 3 or 5 years.

Conclusion

Laparoscopic liver resection for CRLM offers improved short-term outcomes with comparable long-term outcomes when compared to open approach.

Keywords

Minimally Colorectal Cancer Metastases Resection Hepatectomy Liver 

Notes

Compliance with ethical standards

Disclosures

Drs. Ciria, Ocaña, Gómez-Luque, Cipriani, Halls, Fretland, Okuda, Aroori, Briceño, Aldrighetti, Edwin and Abu Hilal have no conflicts of interest or financial ties to disclose.

Supplementary material

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Supplementary material 1 (DOCX 29 kb)
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References

  1. 1.
    Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F (2017) Global patterns and trends in colorectal cancer incidence and mortality. Gut 66:683–691.  https://doi.org/10.1136/gutjnl-2015-310912 CrossRefGoogle Scholar
  2. 2.
    Jones RP, Jackson R, Dunne DFJ, Malik HZ, Fenwick SW, Poston GJ, Ghaneh P (2012) Systematic review and meta-analysis of follow-up after hepatectomy for colorectal liver metastases. Br J Surg 99:477–486.  https://doi.org/10.1002/bjs.8667 CrossRefGoogle Scholar
  3. 3.
    ‘t Lam-Boer J, Ali Al C, Verhoeven RHA, Roumen RMH, Lemmens VEPP, Rijken AM, De Wilt JHW (2015) Large variation in the utilization of liver resections in stage IV colorectal cancer patients with metastases confined to the liver. Eur J Surg Oncol 41:1217–1225.  https://doi.org/10.1016/j.ejso.2015.05.014 CrossRefGoogle Scholar
  4. 4.
    Ahmad A, Reha J, Somasundar P, Espat NJ, Katz SC (2016) Predictors of surgical non-referral for colorectal liver metastases. J Surg Res 205:198–203.  https://doi.org/10.1016/j.jss.2016.06.037 CrossRefGoogle Scholar
  5. 5.
    Martínez-Cecilia D, Cipriani F, Vishal S, Ratti F, Tranchart H, Barkhatov L, Tomassini F, Montalti R, Halls M, Troisi RI, Dagher I, Aldrighetti L, Edwin B, Abu Hilal M (2017) Laparoscopic versus open liver resection for colorectal metastases in elderly and octogenarian patients: a multicenter propensity score based analysis of short- and long-term outcomes. Ann Surg 265:1192–1200.  https://doi.org/10.1097/SLA.0000000000002147 CrossRefGoogle Scholar
  6. 6.
    Cipriani F, Rawashdeh M, Stanton L, Armstrong T, Takhar A, Pearce NW, Primrose J, Abu Hilal M (2016) Propensity score-based analysis of outcomes of laparoscopic versus open liver resection for colorectal metastases. Br J Surg 103:1504–1512.  https://doi.org/10.1002/bjs.10211 CrossRefGoogle Scholar
  7. 7.
    Ciria R, Cherqui D, Geller DA, Briceño J, Wakabayashi G (2016) Comparative short-term benefits of laparoscopic liver resection: 9000 cases and climbing. Ann Surg 263:761–777.  https://doi.org/10.1097/SLA.0000000000001413 CrossRefGoogle Scholar
  8. 8.
    Fretland ÅA, Dagenborg VJ, Bjørnelv GMW, Kazaryan AM, Kristiansen R, Fagerland MW, Hausken J, Tønnessen TI, Abildgaard A, Barkhatov L, Yaqub S, Røsok BI, Bjørnbeth BA, Andersen MH, Flatmark K, Aas E, Edwin B (2018) Laparoscopic versus open resection for colorectal liver metastases: the OSLO-COMET Randomized Controlled Trial. Ann Surg 267:199–207.  https://doi.org/10.1097/SLA.0000000000002353 CrossRefGoogle Scholar
  9. 9.
    Abu Hilal M, Aldrighetti L, Dagher I, Edwin B, Troisi RI, Alikhanov R, Aroori S, Belli G, Besselink M, Briceño J, Gayet B, D’Hondt M, Lesurtel M, Menon K, Lodge P, Rotellar F, Santoyo J, Scatton O, Soubrane O, Sutcliffe R, Van Dam R, White S, Halls MC, Cipriani F, Van der Poel M, Ciria R, Barkhatov L, Gomez-Luque Y, Ocana-Garcia S, Cook A, Buell J, Clavien P-A, Dervenis C, Fusai G, Geller D, Lang H, Primrose J, Taylor M, Van Gulik T, Wakabayashi G, Asbun H, Cherqui D (2017) The Southampton Consensus Guidelines for laparoscopic liver surgery: from indication to implementation. Ann Surg 268:1–18.  https://doi.org/10.1097/SLA.0000000000002524 Google Scholar
  10. 10.
    Buell JF, Cherqui D, Geller DA, O’Rourke N, Iannitti D, Dagher I, Koffron AJ, Thomas M, Gayet B, Han H-S, Wakabayashi G, Belli G, Kaneko H, Ker C-G, Scatton O, Laurent A, Abdalla EK, Chaudhury P, Dutson E, Gamblin C, D’Angelica M, Nagorney D, Testa G, Labow D, Manas D, Poon RT, Nelson H, Martin R, Clary B, Pinson WC, Martinie J, Vauthey J-N, Goldstein R, Roayaie S, Barlet D, Espat J, Abecassis M, Rees M, Fong Y, McMasters KM, Broelsch C, Busuttil R, Belghiti J, Strasberg S, Chari RS, World Consensus Conference on Laparoscopic Surgery (2009) The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg 250(5):825–830CrossRefGoogle Scholar
  11. 11.
    Petrie JC, Grimshaw JM, Bryson A (1995) The Scottish Intercollegiate Guidelines Network Initiative: getting validated guidelines into local practice. Health Bull (Edinb) 53:345–348Google Scholar
  12. 12.
    Simonian R, Laird N (1986) Meta-analysis in clinical trials. Controlled Clinical Trials 7:177–188CrossRefGoogle Scholar
  13. 13.
    Higgins JPT, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560.  https://doi.org/10.1136/bmj.327.7414.557 CrossRefGoogle Scholar
  14. 14.
    Mantel N, Haenszel W (1959) Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 22:719–748Google Scholar
  15. 15.
    Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw 36:1–48CrossRefGoogle Scholar
  16. 16.
    Wallace BC, Dahabreh IJ, Trikalinos TA, Lau J, Trow P, Schmid CH (2012) Closing the gap between methodologists and end-users: r as a computational back-end. J Stat Softw 49:1–15CrossRefGoogle Scholar
  17. 17.
    Wan X, Wang W, Tong T (2014) Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. arXivGoogle Scholar
  18. 18.
    Mala T, Edwin B, Gladhaug I, Fosse E, Søreide O, Bergan A, Mathisen Ø (2002) A comparative study of the short-term outcome following open and laparoscopic liver resection of colorectal metastases. Surg Endosc 16:1059–1063.  https://doi.org/10.1007/s00464-001-9176-5 CrossRefGoogle Scholar
  19. 19.
    Huh JW, Koh YS, Kim HR, Cho CK, Kim YJ (2011) Comparison of laparoscopic and open colorectal resections for patients undergoing simultaneous R0 resection for liver metastases. Surg Endosc 25:193–198.  https://doi.org/10.1007/s00464-010-1158-z CrossRefGoogle Scholar
  20. 20.
    Chen K-Y, Xiang G-A, Wang H-N, Xiao F-L (2011) Simultaneous laparoscopic excision for rectal carcinoma and synchronous hepatic metastasis. Chin Med J 124:2990–2992.  https://doi.org/10.3760/cma.j.issn.0366-6999.2011.19.006 Google Scholar
  21. 21.
    Karagkounis G, Akyuz M, Guerron AD, Yazici P, Aucejo FN, Quintini C, Miller CM, Vogt DP, Fung JJ, Berber E (2016) Perioperative and oncologic outcomes of minimally invasive liver resection for colorectal metastases: a case-control study of 130 patients. Surgery 160:1097–1103.  https://doi.org/10.1016/j.surg.2016.04.043 CrossRefGoogle Scholar
  22. 22.
    Allard M-A, Cunha AS, Gayet B, Adam R, Goere D, Bachellier P, Azoulay D, Ayav A, Navarro F, Pessaux P, Colorectal Liver Metastases-French Study Group (2015) Early and long-term oncological outcomes after laparoscopic resection for colorectal liver metastases: a propensity score-based analysis. Ann Surg 262:794–802.  https://doi.org/10.1097/sla.0000000000001475 CrossRefGoogle Scholar
  23. 23.
    Tohme S, Goswami J, Han K, Chidi AP, Geller DA, Reddy S, Gleisner A, Tsung A (2015) Minimally invasive resection of colorectal cancer liver metastases leads to an earlier initiation of chemotherapy compared to open surgery. J Gastrointest Surg 19:2199–2206.  https://doi.org/10.1007/s11605-015-2962-5 CrossRefGoogle Scholar
  24. 24.
    Langella S, Russolillo N, D’Eletto M, Forchino F, Tesoriere Lo R, Ferrero A (2015) Oncological safety of ultrasound-guided laparoscopic liver resection for colorectal metastases: a case-control study. Updates Surg 67:147–155.  https://doi.org/10.1007/s13304-015-0325-0 CrossRefGoogle Scholar
  25. 25.
    Kubota Y, Otsuka Y, Tsuchiya M, Katagiri T, Ishii J, Maeda T, Tamura A, Kaneko H (2014) Efficacy of laparoscopic liver resection in colorectal liver metastases and the influence of preoperative chemotherapy. World J Surg Oncol 12:351.  https://doi.org/10.1186/1477-7819-12-351 CrossRefGoogle Scholar
  26. 26.
    Guerron AD, Aliyev S, Agcaoglu O, Aksoy E, Taskin HE, Aucejo F, Miller C, Fung J, Berber E (2013) Laparoscopic versus open resection of colorectal liver metastasis. Surg Endosc 27:1138–1143.  https://doi.org/10.1007/s00464-012-2563-2 CrossRefGoogle Scholar
  27. 27.
    Doughtie CA, Egger ME, Cannon RM, Martin RCG, McMasters KM, Scoggins CR (2013) Laparoscopic hepatectomy is a safe and effective approach for resecting large colorectal liver metastases. Am Surg 79:566–571Google Scholar
  28. 28.
    Cannon RM, Scoggins CR, Callender GG, McMasters KM, Martin RCG (2012) Laparoscopic versus open resection of hepatic colorectal metastases. Surgery 152:567–573.  https://doi.org/10.1016/j.surg.2012.07.013 discussion 573–4 CrossRefGoogle Scholar
  29. 29.
    Topal B, Tiek J, Fieuws S, Aerts R, Cutsem E, Roskams T, Prenen H (2012) Minimally invasive liver surgery for metastases from colorectal cancer: oncologic outcome and prognostic factors. Surg Endosc 26:2288–2298.  https://doi.org/10.1007/s00464-012-2176-9 CrossRefGoogle Scholar
  30. 30.
    Abu Hilal M, Underwood T, Zuccaro M, Primrose J, Pearce N (2010) Short- and medium-term results of totally laparoscopic resection for colorectal liver metastases. Br J Surg 97:927–933.  https://doi.org/10.1002/bjs.7034 CrossRefGoogle Scholar
  31. 31.
    Castaing D, Vibert E, Ricca L, Azoulay D, Adam R, Gayet B (2009) Oncologic results of laparoscopic versus open hepatectomy for colorectal liver metastases in two specialized centers. Ann Surg 250:849–855.  https://doi.org/10.1097/SLA.0b013e3181bcaf63 CrossRefGoogle Scholar
  32. 32.
    Iwahashi S, Shimada M, Utsunomiya T, Imura S, Morine Y, Ikemoto T, Arakawa Y, Mori H, Kanamoto M, Yamada S (2014) Laparoscopic hepatic resection for metastatic liver tumor of colorectal cancer: comparative analysis of short- and long-term results. Surg Endosc 28:80–84.  https://doi.org/10.1007/s00464-013-3165-3 CrossRefGoogle Scholar
  33. 33.
    Nachmany I, Pencovich N, Zohar N, Ben-Yehuda A, Binyamin C, Goykhman Y, Lubezky N, Nakache R, Klausner JM (2015) Laparoscopic versus open liver resection for metastatic colorectal cancer. Eur J Surg Oncol 41:1615–1620.  https://doi.org/10.1016/j.ejso.2015.09.014 CrossRefGoogle Scholar
  34. 34.
    Cheung TT, Poon RTP, Yuen WK, Chok KSH, Tsang SHY, Yau T, Chan SC, Lo CM (2013) Outcome of laparoscopic versus open hepatectomy for colorectal liver metastases. ANZ J Surg 83:847–852.  https://doi.org/10.1111/j.1445-2197.2012.06270.x CrossRefGoogle Scholar
  35. 35.
    Inoue Y, Hayashi M, Tanaka R, Komeda K, Hirokawa F, Uchiyama K (2013) Short-term results of laparoscopic versus open liver resection for liver metastasis from colorectal cancer: a comparative study. Am Surg 79:495–501Google Scholar
  36. 36.
    Hasegawa Y, Nitta H, Sasaki A, Takahara T, Itabashi H, Katagiri H, Otsuka K, Nishizuka S, Wakabayashi G (2015) Long-term outcomes of laparoscopic versus open liver resection for liver metastases from colorectal cancer: a comparative analysis of 168 consecutive cases at a single center. Surgery 157:1065–1072.  https://doi.org/10.1016/j.surg.2015.01.017 CrossRefGoogle Scholar
  37. 37.
    Topal H, Tiek J, Aerts R, Topal B (2012) Outcome of laparoscopic major liver resection for colorectal metastases. Surg Endosc 26:2451–2455.  https://doi.org/10.1007/s00464-012-2209-4 CrossRefGoogle Scholar
  38. 38.
    Tranchart H, Fuks D, Viganò L, Ferretti S, Paye F, Wakabayashi G, Ferrero A, Gayet B, Dagher I (2016) Laparoscopic simultaneous resection of colorectal primary tumor and liver metastases: a propensity score matching analysis. Surg Endosc 30:1853–1862.  https://doi.org/10.1007/s00464-015-4467-4 CrossRefGoogle Scholar
  39. 39.
    Ratti F, Catena M, Di Palo S, Staudacher C, Aldrighetti L (2016) Impact of totally laparoscopic combined management of colorectal cancer with synchronous hepatic metastases on severity of complications: a propensity-score-based analysis. Surg Endosc 30(11):4934–4945.  https://doi.org/10.1007/s00464-016-4835-8 CrossRefGoogle Scholar
  40. 40.
    Lin Q, Ye Q, Zhu D, Wei Y, Ren L, Zheng P, Xu P, Ye L, Lv M, Fan J, Xu J (2015) Comparison of minimally invasive and open colorectal resections for patients undergoing simultaneous R0 resection for liver metastases: a propensity score analysis. Int J Colorectal Dis 30:385–395.  https://doi.org/10.1007/s00384-014-2089-2 CrossRefGoogle Scholar
  41. 41.
    Jung KU, Kim HC, Cho YB, Kwon CHD, Yun SH, Heo JS, Lee WY, Chun H-K (2014) Outcomes of simultaneous laparoscopic colorectal and hepatic resection for patients with colorectal cancers: a comparative study. J Laparoendosc Adv Surg Tech 24:229–235.  https://doi.org/10.1089/lap.2013.0475 CrossRefGoogle Scholar
  42. 42.
    Hu M-G, Ou-yang C-G, Zhao G-D, Xu D-B, Liu R (2012) Outcomes of open versus laparoscopic procedure for synchronous radical resection of liver metastatic colorectal cancer: a comparative study. Surg Laparosc Endosc Percutan Tech 22:364–369.  https://doi.org/10.1097/SLE.0b013e31825af6b2 CrossRefGoogle Scholar
  43. 43.
    Fretland ÅA, Dagenborg VJ, Bjørnelv GMW, Kazaryan AM, Kristiansen R, Fagerland MW, Hausken J, Tønnessen TI, Abildgaard A, Barkhatov L, Yaqub S, Røsok BI, Bjørnbeth BA, Andersen MH, Flatmark K, Aas E, Edwin B, Oslo-CoMet Study Group (2017) Laparoscopic versus open resection for colorectal liver metastases: the OSLO-COMET Randomized Controlled Trial. Ann Surg 267(2):199–207.  https://doi.org/10.1097/sla.0000000000002353 CrossRefGoogle Scholar
  44. 44.
    Untereiner X, Cagniet A, Memeo R, Tzedakis S, Piardi T, Severac F, Mutter D, Kianmanesh R, Marescaux J, Sommacale D, Pessaux P (2016) Laparoscopic hepatectomy versus open hepatectomy for colorectal cancer liver metastases: comparative study with propensity score matching. Hepatobiliary Surg Nutr 5:290–299.  https://doi.org/10.21037/hbsn.2015.12.06 CrossRefGoogle Scholar
  45. 45.
    Lewin JW, O’Rourke NA, Chiow AKH, Bryant R, Martin I, Nathanson LK, Cavallucci DJ (2016) Long-term survival in laparoscopic vs open resection for colorectal liver metastases: inverse probability of treatment weighting using propensity scores. HPB (Oxford) 18:183–191.  https://doi.org/10.1016/j.hpb.2015.08.001 CrossRefGoogle Scholar
  46. 46.
    Beppu T, Wakabayashi G, Hasegawa K, Gotohda N, Mizuguchi T, Takahashi Y, Hirokawa F, Taniai N, Watanabe M, Katou M, Nagano H, Honda G, Baba H, Kokudo N, Konishi M, Hirata K, Yamamoto M, Uchiyama K, Uchida E, Kusachi S, Kubota K, Mori M, Takahashi K, Kikuchi K, Miyata H, Takahara T, Nakamura M, Kaneko H, Yamaue H, Miyazaki M, Takada T (2015) Long-term and perioperative outcomes of laparoscopic versus open liver resection for colorectal liver metastases with propensity score matching: a multi-institutional Japanese study. J Hepato-Biliary Pancreat Sci 22:711–720.  https://doi.org/10.1002/jhbp.261 CrossRefGoogle Scholar
  47. 47.
    de’Angelis N, Eshkenazy R, Brunetti F, Valente R, Costa M, Disabato M, Salloum C, Compagnon P, Laurent A, Azoulay D (2015) Laparoscopic versus open resection for colorectal liver metastases: a single-center study with propensity score analysis. J Laparoendosc Adv Surg Tech 25:12–20.  https://doi.org/10.1089/lap.2014.0477 CrossRefGoogle Scholar
  48. 48.
    Qiu J, Chen S, Pankaj P, Wu H (2014) Laparoscopic hepatectomy is associated with considerably less morbidity and a long-term survival similar to that of the open procedure in patients with hepatic colorectal metastases. Surg Laparosc Endosc Percutan Tech 24:517–522.  https://doi.org/10.1097/SLE.0b013e31829cec2b Google Scholar
  49. 49.
    Montalti R, Berardi G, Laurent S, Sebastiani S, Ferdinande L, Libbrecht LJ, Smeets P, Brescia A, Rogiers X, De Hemptinne B, Geboes K, Troisi RI (2014) Laparoscopic liver resection compared to open approach in patients with colorectal liver metastases improves further resectability: oncological outcomes of a case-control matched-pairs analysis. Eur J Surg Oncol 40:536–544.  https://doi.org/10.1016/j.ejso.2014.01.005 CrossRefGoogle Scholar
  50. 50.
    Qiu J, Chen S, Pankaj P, Wu H (2013) Laparoscopic hepatectomy for hepatic colorectal metastases: a retrospective comparative cohort analysis and literature review. PLoS ONE 8:e60153.  https://doi.org/10.1371/journal.pone.0060153 CrossRefGoogle Scholar
  51. 51.
    Nguyen KT, Marsh JW, Tsung A, Steel JJL, Gamblin TC, Geller DA (2011) Comparative benefits of laparoscopic vs open hepatic resection: a critical appraisal. Arch Surg 146:348–356.  https://doi.org/10.1001/archsurg.2010.248 CrossRefGoogle Scholar
  52. 52.
    Cipriani F, Shelat VG, Rawashdeh M, Francone E, Aldrighetti L, Takhar A, Armstrong T, Pearce NW, Abu Hilal M (2015) Laparoscopic parenchymal-sparing resections for nonperipheral liver lesions, the diamond technique: technical aspects, clinical outcomes, and oncologic efficiency. J Am Coll Surg 221:265–272.  https://doi.org/10.1016/j.jamcollsurg.2015.03.029 CrossRefGoogle Scholar
  53. 53.
    Abu Hilal M, Di Fabio F, Abu Salameh M, Pearce NW (2012) Oncological efficiency analysis of laparoscopic liver resection for primary and metastatic cancer: a single-center UK experience. Arch Surg 147:42–48.  https://doi.org/10.1001/archsurg.2011.856 CrossRefGoogle Scholar
  54. 54.
    Yamashita S, Sheth RA, Niekamp AS, Aloia TA, Chun YS, Lee JE, Vauthey J-N, Conrad C (2016) Comprehensive complication index predicts cancer-specific survival after resection of colorectal metastases independent of RAS mutational status. Ann Surg.  https://doi.org/10.1097/sla.0000000000002018 Google Scholar
  55. 55.
    McPhail MJW, Scibelli T, Abdelaziz M, Titi A, Pearce NW, Abu Hilal M (2009) Laparoscopic versus open left lateral hepatectomy. Expert Rev Gastroenterol Hepatol 3:345–351.  https://doi.org/10.1586/egh.09.36 CrossRefGoogle Scholar
  56. 56.
    Cipriani F, Rawashdeh M, Ahmed M, Armstrong T, Pearce NW, Abu Hilal M (2015) Oncological outcomes of laparoscopic surgery of liver metastases: a single-centre experience. Updates Surg 67:185–191.  https://doi.org/10.1007/s13304-015-0308-1 CrossRefGoogle Scholar
  57. 57.
    Yamashita S, Venkatesan AM, Mizuno T, Aloia TA, Chun YS, Lee JE, Vauthey J-N, Conrad C (2017) Remnant liver ischemia as a prognostic factor for cancer-specific survival after resection of colorectal liver metastases. JAMA Surg 152:e172986.  https://doi.org/10.1001/jamasurg.2017.2986 CrossRefGoogle Scholar
  58. 58.
    Hozo SP, Djulbegovic B, Hozo I (2005) Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 5:13.  https://doi.org/10.1186/1471-2288-5-13 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Ruben Ciria
    • 1
    Email author
  • Sira Ocaña
    • 2
  • Irene Gomez-Luque
    • 1
  • Federica Cipriani
    • 3
    • 4
  • Mark Halls
    • 4
  • Åsmund Avdem Fretland
    • 5
    • 6
    • 7
  • Yukihiro Okuda
    • 1
    • 8
  • Somaiah Aroori
    • 9
  • Javier Briceño
    • 1
  • Luca Aldrighetti
    • 3
  • Bjorn Edwin
    • 5
    • 6
    • 7
  • Mohammed Abu Hilal
    • 4
    Email author
  1. 1.Unit of Hepatobiliary Surgery and Liver Transplantation, University Hospital Reina Sofía, IMIBICUniversity of CordobaCordobaSpain
  2. 2.Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, University ClinicUniversity of NavarraPamplonaSpain
  3. 3.Hepatobiliary Surgery DivisionSan Raffaele HospitalMilanItaly
  4. 4.Department of Hepato-Biliary and Pancreatic SurgeryUniversity Hospital Southampton NHS Foundation TrustSouthamptonUK
  5. 5.Department of HPB SurgeryOslo University Hospital-RikshospitaletOsloNorway
  6. 6.Institute of Clinical Medicine, Medical FacultyUniversity of OsloOsloNorway
  7. 7.The Intervention CentreOslo University HospitalOsloNorway
  8. 8.Department of Surgery, Graduate School of MedicineKyoto UniversityKyotoJapan
  9. 9.Unit of Hepatobiliary and Pancreatic SurgeryDerriford HospitalPlymouthUK

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