Abstract
Background
The laparoscopic approach in the treatment of mid- or low-rectal cancer is still controversial. Compared with open surgery, laparoscopic resection of extraperitoneal cancer is associated with improved short-time non-oncological outcomes, although high-level evidence showing similar short- and long-term oncological outcomes is scarce.
Objective
The aim of our paper is to study the oncological and non-oncological outcomes of laparoscopic versus open surgery for extraperitoneal rectal cancer.
Data sources
A systematic review of MedLine, EMBASE, and CENTRAL from January 1990 to October 2020 was performed by combining various key words.
Study selection
Only randomized controlled trials (RCTs) comparing laparoscopic versus open surgery for extraperitoneal rectal cancer were included. The quality of RCTs was assessed using the Cochrane reviewer’s handbook. This meta-analysis was based on the recommendation of the Preferred Reporting Items for Systematic Reviews and Meta-Analysis guidelines.
Intervention(s)
This study analyzes laparoscopic versus open surgery for extraperitoneal rectal cancer.
Main outcome measures
Primary outcomes were oncological parameters.
Results
Fifteen RCTs comprising 4,411 patients matched the selection criteria. Meta-analysis showed a significant difference between laparoscopic and open surgery in short-time non-oncological outcomes. Although laparoscopic approach increased operation time, it decreases significantly the blood loss and length of hospital stay. No significant difference was noted regarding short- and long-term oncological outcomes, but 4 and 5 years disease-free survival were statistically higher in the open group.
Limitations
There are still questions about the long-term oncological outcomes of laparoscopic surgery for extraperitoneal rectal cancer being comparable to the open technique.
Conclusions
Considering that all surgical resections have been performed in high volume centers by expert surgeons, the minimally invasive surgery in patients with extraperitoneal cancer could still be not considered equivalent to open surgery in terms of oncological radicality.
Similar content being viewed by others
References
Brenner H, Bouvier AM, Foschi R, Hackl M, Larsen IK, Lemmens V, Mangone L, Francisci S, EUROCARE Working Group (2012) Progress in colorectal cancer survival in Europe from the late 1980s to the early 21st century: the EUROCARE study. Int J Cancer 131:1649–1658
Lacy AM, García-Valdecasas JC, Delgado S, Castells A, Taurá P, Piqué JM, Visa J (2002) Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomized trial. Lancet 359:2224–2229
The Clinical Outcomes of Surgical Therapy Study Group (2004) A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med 350:2050–2059
Guillou PJ, Quirke P, Thorpe H, Walker J, Jayne DG, Smith AMH, Heath RM, Brown JM (2005) Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomized controlled trial. Lancet 365:1718–1726
Green BL, Marshall HC, Collinson F, Quirke P, Guillou P, Jayne DG, Brown JM (2013) Long-term follow-up of the Medical Research Council CLASICC trial of conventional versus laparoscopically assisted resection in colorectal cancer. Br J Surg 100:75–82
Veldkamp R, Kuhry E, Hop WC, Jeekel J, Kazemier G, Bonjer HJ, Haglind E, Påhlman L, Cuesta MA, Msika S, Morino M, Lacy AM, COLOR (2005) Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomized trial. Lancet Oncol 6:477–484
Kaltoft B, Gögenur I, Rosenberg J (2011) Reduced length of stay and convalescence in laparoscopic vs open sigmoid resection with traditional care: a double blinded randomized clinical trial. Colorectal Dis 13:e123–e130
The COST Group, Nelson H, Sargent DJ, Wieand HS, Fleshman J, Anvari M, Stryker SJ, Beart RW Jr, Hellinger M, Flanagan R Jr, Peters W, Ota D (2004) A comparison of laparoscopically-assisted and open colectomy for colon cancer. N Engl J Med 350:2050–2059
Veldcamp R, Kuhry E, Jeekel HWC, J, Kazemier G, Bonjer HJ, Haglind E, Påhlman L, Cuesta MA, Msika S, Morino M, Lacy AM, COLOR (2005) Colon cancer laparoscopic or open resection study group (COLOR). Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol 6:477–484
Kim NK, Aahn TW, Park JK et al (2002) Assessment of sexual and voiding function after total mesorectal excision with pelvic autonomic nerve preservation in males with rectal cancer. Dis Colon Rectum 45:1178–1185
Kim JY, Kim NK, Lee KY, Hur H, Min BS, Kim JH (2012) A comparative study of voiding and sexual function after total mesorectal excision with autonomic nerve preservation for rectal cancer: laparoscopic versus robotic surgery. Ann Surg Oncol 19(8):2485–2493. https://doi.org/10.1245/s10434-012-2262-1 (Epub 2012 Mar 21 PMID: 22434245)
Jayne DG, Brown JM, Thorpe H et al (2005) Bladder and sexual function following resection for rectal cancer in a randomized clinical trial of laparoscopic versus open technique. Br J Surg 92:1124–1132
Asoglu O, Matlim T, Karanlik H et al (2009) Impact of laparoscopic surgery on bladder and sexual function after total mesorectal excision for rectal cancer. Surg Endosc 23:296–303
Liang J, Lai H, Lee P (2007) Laparoscopic pelvic autonomic nerve-preserving surgery for patients with lower rectal cancer after chemoradiation therapy. Ann Surg Oncol 14:1285–1287
Morino M, Parini U, Allaix ME et al (2009) Male sexual and urinary function after laparoscopic total mesorectal excision. Surg Endosc 23:1233–1240
Giuratrabocchetta S, Formisano G, Salaj A, Opocher E, Ferraro L, Toti F, Bianchi PP (2021) Update on robotic total mesorectal excision for rectal cancer. J Pers Med 8;11(9):900. https://doi.org/10.3390/jpm11090900. PMID: 34575677; PMCID: PMC8472541
Delaney CP, Kiran RP, Senagore AJ, Brady K, Fazio VW (2003) Case-matched comparison of clinical and financial outcome after laparoscopic or open colorectal surgery. Ann Surg 238:67–72
Araujo SEA, Sousa Jr AHDS, Campos FGCMD, Habr-Gama A, Dumarco RB, Caravatto PPDP, Nahas SC, Silva da JH, Kiss DR, Gama-Rodrigues JJ (2003) Conventional approach x laparoscopic abdominoperineal resection for rectal cancer treatment after neoadjuvant chemoradiation: results of a prospective randomized trial. Rev Hosp Clin 58:133–140
Jeong SY, Park JW, Nam BH, Kim S, Kang SB (2014) Open versus laparoscopic surgery for mid-rectal or low-rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): survival outcomes of an open-label, non-inferiority, randomized controlled trial. Lancet Oncol 15:767–774
Stevenson ARL, Solomon MJ, Lumley JW, Hewett P, Clouston AD, Gebski VJ, Davies L, Wilson K, Hague W, Simes J, for the ALaCaRT investigators (2015) Effect of laparoscopic-assisted resection vs open resection on pathological outcomes in rectal cancer the ALaCaRT randomized clinical trial. J Am Med Assoc 314:1356–1363
Stevenson ARL, Solomon MJ, Brown C, Lumley JW, Hewett P, Clouston AD, Gebski VJ, Wilson K, Hague W, John S, on behalf of AGITG ALaCaRT investigators (2019) Disease-free survival and local recurrence after laparoscopic assisted resection or open resection for rectal cancer the Australasian laparoscopic cancer of the rectum randomized clinical trial. Ann Surg 269:596–602
Zhou ZG, Hu M, Li Y, lei WZ, Yu YY, Cheng Z, Li L, Shut Y, Wang TC (2004) Laparoscopic versus open total mesorectal excision with anal sphincter preservation for low rectal cancer. Surg Endosc 18:1211–1215
Lujan J, Valero G, Hernandez Q, Sanchez A, Frutos MD, Parrilla P (2009) Randomized clinical trial comparing laparoscopic and open surgery in patients with rectal cancer. Br J Surg 96:982–989
Pechlivanides G, Gouvas N, Tsiaoussis J, Tzortzinis A, Tzardi M, Moutafidis M, Dervenis C, Xynos E (2007) Lymph node clearance after total mesorectal excision for rectal cancer: laparoscopic versus open approach. Dig Dis 25:94–99
Park IJ, Choi GS, Lim KH, Kang BM, Jun SH (2009) Laparoscopic resection of extraperitoneal rectal cancer: a comparative analysis with open resection. Surg Endosc 23:1818–1824
Baik SH, Gincherman M, Mutch MG, Birnbaum EH, Fleshman JW (2011) Laparoscopic vs open resection for patients with rectal cancer: comparison of perioperative outcomes and long-term survival. Dis Colon Rectum 54:6–14
Ng SSM, Leung KL, Lee JFY, Yiu RYC, Li JCM, Teoh AYB, Leung WW (2008) Laparoscopic-assisted versus open abdominoperineal resection for low rectal cancer: a prospective randomized trial. Ann Surg Onc 15:2418–2425
Ng SSM, Lee JFY, Yiu RYC, Li JCM, Hon SSF, Mak TWC, Ngo DKY, Leung WW, Leung KL (2014) Laparoscopic-assisted versus open total mesorectal excision with anal sphincter preservation for mid and low rectal cancer: a prospective, randomized trial. Surg Endosc 28:297–306
Bonjer HJ, Deijen CL, Abis GA, Van der Pas MHGM, de Lange-de Klerk ESM, Lacy AM, Bemelman WA, Andersson J, Angenete E, Rosenberg J, Fuerst A, Haglind E (2015) A randomized trial of laparoscopic versus open surgery for rectal cancer. N Engl J Med 372:1324–1332
Li S, Jiang F, Tu J, Zheng X (2015) Long-term oncologic outcomes of laparoscopic versus open surgery for middle and lower rectal cancer. PLoS ONE 10:e0135884
Fleshman J, Branda M, Sargent DJ, Boller AM, George V, Abbas M, Peters WR Jr, Maun D, Chang G, Herline A, Fichera A, Mutch M, Wexner S, Whiteford M, Marks J, Birnbaum E, Margolin D, Larson D, Marcello P, Posner M, Read T, Monson J, Wren SM, Pisters PWT, Nelson H (2015) Effect of laparoscopic-assisted resection vs open resection of stage II or III rectal cancer on pathologic outcomes: the ACOSOG Z6051 randomized clinical trial. JAMA 314:1346–1355
Fleshman J, Branda M, Sargent DJ, Boller AM, George V, Abbas M, Peters WR Jr, Maun D, Chang G, Herline A, Fichera A, Mutch M, Wexner S, Whiteford M, Marks J, Birnbaum E, Margolin D, Larson D, Marcello P, Posner M, Read T, Monson JRT, Wren SM, Pisters PWT, Nelson H (2019) Disease-free survival and local recurrence for laparoscopic resection compared to open resection of stage II/III rectal cancer: follow-up results of the ACOSOG Z6051 randomized controlled trial Ann. Surg 269:589–595
Panic N, Leoncini E, de Belvis G, Ricciardi W, Boccia S (2013) Evaluation of the endorsement of the preferred reporting items for systematic reviews and meta-analysis (PRISMA) statement on the quality of published systematic review and meta-analyses. PLoS One 8:e83138
Higgins JPT, Green S (2011) Cochrane handbook for systematic reviews of interventions, version 5.1.0. Updated March 2011. The Cochrane Collaboration
Faggiano F, Barbone F, Donato F (2005) Manuale di Epidemiologia per la sanità pubblica, pp 315–316
Kang SB, Park JW, Jeong SY, Nam BH, Choi HS, Kim DW, Lim SB, Lee TG, Kim DY, Kim JS, Chang HJ, Lee HS, Kim SY, Jung KH, Hong YS, Kim JH, Sohn DK, Kim DH, Oh JH (2010) Open versus laparoscopic surgery for mid or low rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): short-term outcomes of an open-label randomized controlled trial. Lancet Oncol 11:637–645
Keskin M, Akici M, Agcaoglu O, Yegen G, Saglam E, Bugra D, Bulut M, Balik E (2016) Open versus laparoscopic surgery for mid or low rectal cancer: single-center results of 587 cases. Surg Laparosc Endosc Percutan Tech 26:e62–e68
Jacobs M, Verdeja JC, Goldstein HS (1991) Minimally invasive colon resection (laparoscopic colectomy). Surg Laparosc Endosc 1:144–150
Perdawood SK, Thinggaard BS, Bjoern MX (2018) Effect of transanal total mesorectal excision for rectal cancer: comparison of short-term outcomes with laparoscopic and open surgeries. Surg Endosc 32:2312–2321
Bonjer HJ, Hop WC, Nelson H, Sargent DJ, Lacy AM, Castells A, GUillou PJ, Thorpe H, Brown J, Delgado S, Kuhry E, Pahlman L (2007) Laparoscopically assisted vs open colectomy for colon cancer: a meta-analysis. Arch Surg 142:298–303
Wilson MZ, Hollenbeak CS, Stewart DB (2014) Laparoscopic colectomy is associated with lower incidence of postoperative complications than open colectomy: a propensity score-matched cohort analysis. Color Dis 16:382–389
Zheng J, Feng X, Yang Z, Hu W, Luo Y, Li Y (2017) The comprehensive therapeutic effects of rectal surgery are better in laparoscopy: a systematic review and meta-analysis. Oncotarget 8:12717–12729
Martinez-Perez A, Carra MC, Brunetti F, de Angelis N (2017) Short-term clinical outcomes of laparoscopic vs open rectal excision for rectal cancer: a systematic review and meta-analysis. World J Gastroenterol 23:7906–7916
Creavin B, Kelly ME, Ryan E, Winter DC (2017) Meta-analysis of the impact of surgical approach on the grade of mesorectal excision in rectal cancer. Br J Surg 104:1609–1619
Kang SB, Kang SB, Park JW, Jeong SY, Nam BH, Choi HS, Kim DW, Lim SB, Lee TG, Kim DY, Kim JS, Chang HJ, Lee HS, Kim SY, Jung KH, Hong YS, Kim JH, Sohn DK, Kim DH, Oh JH (2010) Open versus laparoscopic surgery for mid or low rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): short-term outcomes of an open-label randomized controlled trial. Lancet Oncol 11:637–645
Van der Pas MH, Haglind E, Cuesta MA, Furst A, Lacy AM, Hop WC, Bonjer HJ (2013) Laparoscopic versus open surgery for rectal cancer (COLOR II): short-term outcomes of a randomised, phase 3 trial. Lancet Oncol 14:210–218
Arteaga Gonzalez I, Diaz Luis H, Martin Malagon A, López-Tomasetti Fernández EM, Arranz Duran J, Carrillo Pallares A (2006) A comparative clinical study of short-term results of laparoscopic surgery for rectal cancer during the learning curve. Int J Colorectal Dis 21:590–595
Fujii S, Ishibe A, Ota M, Yamagishi S, Watanabe K, Watanabe J, Kanazawa A, Ichikawa Y, Oba M, Morita S, Hashiguchi Y, Kunisaki C, Endo I (2014) Short-term results of a randomized study between laparoscopic and open surgery in elderly colorectal cancer patients. Surg Endosc 28:466–476
Gong J, Shi DB, Li XX, Cai AJ, Guan ZQ, Xu Y (2012) Short-term outcomes of laparoscopic total mesorectal excision compared to open surgery. World J Gastroenterol 18:7308–7313
Chen K, Cao G, Chen B, Wang M, Xu X, Cai W, Xu Y, Xiong M (2017) Laparoscopic versus open surgery for rectal cancer: a meta-analysis of classic randomized controlled trials and high quality nonrandomized studies in the last 5 years. Int J Surg 39:1–10
Vennix S, Pelzers L, Bouvy N, Bouvy N, Beets GL, Pierie JP, Wiggers T, Breukink S (2014) Laparoscopic versus open total mesorectal excision for rectal cancer. Cochrane Database Syst Rev. CD005200
Zhao JK, Chen NZ, Zheng JB, He S, Sun XJ (2014) Laparoscopic versus open surgery for rectal cancer: results of a systematic review and meta-analysis on clinical efficacy. Mol Clin Oncol 2:1097–1102
Zhou ZG, Hu M, Li Y, Lei WZ, Yu YY, Cheng Z, li L, Shu Y, Wang TC (2004) Laparoscopic vs open total mesorectal excision with anal sphincter preservation for low rectal cancer. Surg Endosc 18:1211–1215
Breukink S, Pierie J, Wiggers T (2006) Laparoscopic versus open total mesorectal excision for rectal cancer. Cochrane Database Syst Rev CD005200
Simillis C, Lal N, Thoukididou S, Kontovounisios C, Smith J, Hompes R, Adamina M, Tekkis P (2019) Open versus laparoscopic versus robotic versus transanal mesorectal excision for rectal cancer: a systematic review and network meta-analysis. Annals of Surgery Ann of Surg 270:59–68
Krishnamurty DM, Wise PE (2016) Importance of surgical margins in rectal cancer. J Surg Oncol 113:323–332
Park IJ, Kim JC (2010) Adequate length of the distal resection margin in rectal cancer: from the oncological point of view. J Gastrointest Surg 14:1331–1337
Bernstein TE, Endreseth BH, Romundstad P, Wibe A (2012) Norwegian colorectal cancer registry. What is a safe distal resection margin in rectal cancer patients treated by low anterior resection without preoperative radiotherapy? Colorectal Dis 14:e48–e55
Kang DW, Kwak HD, Sung NS, Yang IS, Baek SJ, Kwak JM, Kim J, Kim SH (2017) Oncologic outcomes in rectal cancer patients with a ≤1-cm distal resection margin. Int J Colorectal Dis 32:325–332
Kuvshinoff B, Maghfoor I, Miedema B, Bryer M, Westgate S, Wilkes J, Ota D (2001) Distal margin requirements after preoperative chemoradiotherapy for distal rectal carcinomas: are ≤ 1 cm distal margins sufficient? Ann Surg Oncol 8:163–169
Moore HG, Riedel E, Minsky BD, Saltz L, Paty P, Wong D, Cohen AM, Guillem JG (2003) Adequacy of 1 cm distal margin after restorative rectal cancer resection with sharp mesorectal excision and preoperative combined-modality therapy. Ann Surg Oncol 10:80–85
Grosek J, Velenik V, Edhemovic I, Omejc M (2016) The influence of the distal resection margin length on local recurrence and long-term survival in patients with rectal cancer after chemoradiotherapy and Sphincter-preserving rectal resection. Radiol Oncol 51:169–177
Kwak JY, Kim CW, Lim SB, Yu CS, Kim TW, Kim JH, Jang SJ, Kim JC (2012) Oncologically safe distal resection margins in rectal cancer patients treated with chemoradiotherapy. J Gastrointest Surg 16:1947–1954
Vernava AM, Moran M, Rothenberger DA, Wong WD (1992) A prospective evaluation of distal margins in carcinoma of the rectum. Surg Gynecol Obstet 175:333–336
Awwad G, Tou S, Rieger N (2013) Prognostic significance of lymph node yield after long-course preoperative radiotherapy in patients with rectal cancer: a systematic review. Colorect Dis 15:394–403
Ong MLH, Schofield JB (2016) Assessment of lymph node involvement in colorectal cancer. World J Gastrointest Surg 8:179–192
Nienhüser H, Heger P, Schmitz R, Kulu Y, Diener MK, Klose J, Shneider M, Muller-Stich BP, Ulrich A, Buchler MW, Mihaljevic AL, Schmidt T (2018) Short- and long-term oncological outcome after rectal cancer surgery: a systematic review and meta-analysis comparing open versus laparoscopic rectal cancer surgery. J Gastrointest Surg 22:1418–1433
Munini M, Popeskou SG, Galetti K, Roesel R, Mongelli F, Christoforidis D. Transanal (TaTME) vs. laparoscopic total mesorectal excision for mid and low rectal cancer: a propensity score-matched analysis of early and long-term outcomes. Int J Colorectal Dis. 2021 Oct;36(10):2271–2279. https://doi.org/10.1007/s00384-021-04019-0. Epub 2021 Sep 1. PMID: 34467413.
Aubert M, Mege D, Panis Y (2020) Total mesorectal excision for low and middle rectal cancer: laparoscopic versus transanal approach-a meta-analysis. Surg Endosc 34(9):3908–3919. https://doi.org/10.1007/s00464-019-07160-8 (Epub 2019 Oct 15 PMID: 31617090)
Schnitzbauer V, Gerken M, Benz S, Volkel V, Draeger T, Furst A, Klinkhammer Schalke M (2020) Laparoscopic and open surgery in rectal cancer patients in Germany: short and long-term results of a large-year population-based cohort. Surg endosc 34:1132–1141
Giuliani A, Colozzi S, de Santis G, Sista F, Cianca G, Gentile E, Leardi S, Amicucci G (2015) Reconstruction of Scrotal Sac and Penis with Biological Prosthesis and Vacuum Therapy. Plast Reconstr Surg Glob Open 5;3(5):e394
Bruera G, Giuliani A, Romano L, Chiominto A, Di Sibio A, Mastropietro S, Cosenza P, Ricevuto E, Schietroma M, Carlei F; Oncology Network ASL1 Abruzzo (2019) Poorly differentiated neuroendocrine rectal carcinoma with uncommon immune-histochemical features and clinical presentation with a subcutaneous metastasis, treated with first line intensive triplet chemotherapy plus bevacizumab FIr-B/FOx regimen: an experience of multidisciplinary management in clinical practice. BMC Cancer 19(1):960
Netto J, Jansen-Winkeln V, Thieme R, Eckardt J, Bae YJ, Willenberg A, Huppert S, Lyros O, Niebisch S, Allecke F, Kreuser N, Kratzsch J, Kaiser T, Ceglarek U, Thiery J, Gockel I (2019) Stress biomarkers in minimally invasive and conventional colorectal resection. Acta Chir Belg 119:152–161
Pessia B, Romano L, Giuliani A, Lazzarin G, Carlei F, Schietroma M (2020) Squamous cell anal cancer: Management and therapeutic options. Ann Med Surg (Lond) 12;55:36-46
Stead ML, Brown JM, Bosanquet N, Franks PJ, Guillou PJ, Quirke P, Jayne D, Monson JR, Webb AV (2000) Assessing the relative costs of standard open surgery and laparoscopic surgery in colorectal cancer in a randomized controlled trial in the United Kingdom. Crit Rev Oncol Hematol 33:99–103
Biondi A, Grosso G, Mistretta A, Marventano S, Toscano C, Drago F, Gangi S, Basile F (2013) Laparoscopic vs. open approach for colorectal cancer: evolution over time of minimal invasive surgery. BMC Surg 13:S12
Row D, Weiser MR (2010) An update on laparoscopic resection for rectal cancer. Cancer Control 17:16–24
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Schietroma, M., Romano, L., Apostol, A.I. et al. Mid- and low-rectal cancer: laparoscopic vs open treatment—short- and long-term results. Meta-analysis of randomized controlled trials. Int J Colorectal Dis 37, 71–99 (2022). https://doi.org/10.1007/s00384-021-04048-9
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00384-021-04048-9