Skip to main content
SpringerLink
Log in

Controversies in Surgical Oncology: Does the Minimally Invasive Approach for Rectal Cancer Provide Equivalent Oncologic Outcomes Compared with the Open Approach?

  • Colorectal Cancer
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

Compared with open surgery, minimally invasive surgery for colon cancer has been shown to improve short-term outcomes and yield equivalent long-term oncologic results. It remains to be seen if oncologic outcomes for the minimally invasive approach for rectal cancer are equivalent to traditional open rectal resection.

Methods

We conducted a systematic review of Medline, SCOPUS, and Cochrane databases. Relevant studies were selected using Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Five key questions comparing minimally invasive and open oncologic outcomes for rectal cancer were specifically analyzed. A meta-analysis was not done due to heterogeneity of studies.

Results

Forty-five studies met inclusion criteria, including six randomized controlled trials. The laparoscopic approach to rectal resection was not more likely than the traditional open approach to have clear circumferential and distal margins, a complete total mesorectal excision grade, ≥ 12 lymph nodes in the resected specimen, reduced local recurrence rates, or reduced overall survival rates. Two randomized trials revealed that successful laparoscopic resection was not noninferior to open.

Conclusions

Caution should be exercised when choosing surgical options for rectal cancer. Results of randomized trials could not prove that short-term oncologic outcomes of laparoscopic surgery were equivalent to those after open surgery even when performed by surgeons with laparoscopic expertise. However, reported long-term data have not shown a difference in outcomes between laparoscopic and open surgery. Future advances in minimally invasive technology may improve oncologic margins but these will require careful study and scrutiny.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

References

  1. Veldkamp R, Kuhry E, Hop WC, et al. Colon cancer Laparoscopic or Open Resection Study Group (COLOR). Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomized trial. Lancet Oncol. 2005;6:477–84.

    Article  PubMed  Google Scholar 

  2. Fleshman J, Sargent DJ, Green E, et al. Laparoscopic colectomy for cancer is Not inferior to open surgery based on 5-year data from the COST study group trial. Ann Surg. 2007;246:655–64.

    Article  PubMed  Google Scholar 

  3. Guillou PJ, Quirke P, Thorpe H, et al. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet. 2005;365(9472):1718–26.

    Article  PubMed  Google Scholar 

  4. Jayne DG, Thorpe HC, Copeland J, Quirke P, Brown JM, Guillou PJ. Five-year follow-up of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg. 2010;97:1638–45.

    Article  CAS  PubMed  Google Scholar 

  5. Bagshaw PF, Allardyce RA, Frampton CM, et al. Long-term outcomes of the Australasian randomized clinical trial comparing laparoscopic and conventional open surgical treatments for colon cancer. The Australasian Laparoscopic Colon Cancer Study Trial. Ann Surg. 2012;256:915–9.

    Article  PubMed  Google Scholar 

  6. van der Sijp M, Bastiaannet E, Mesker WE, et al. Differences between colon and rectal cancer in complications, short-term survival and recurrences. Int J Colorectal Dis. 2016;31(10):1683–91.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Lujan J, Valero G, Hernandez Q, Sanchez A, Frutos MD, Parrilla P. Randomized clinical trial comparing laparoscopic and open surgery in patients with rectal cancer. Br J Surg. 2009;96:982–9.

    Article  CAS  PubMed  Google Scholar 

  8. Liang X, Hou S, Liu H, et al. Effectiveness and safety of laparoscopic resection versus open surgery in patients with rectal cancer: a randomized, controlled trial from China. J Laparoendosc Adv Surg Tech A. 2011;21:381–5.

    Article  PubMed  Google Scholar 

  9. Kang SB, Park JW, Jeong SY, et al. 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. 2010;11:637–45.

    Article  PubMed  Google Scholar 

  10. Jeong SY, Park JW, Nam BH, et al. Open versus laparoscopic surgery for mid-rectal or low-rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): survival outcomes of an open-label, non-inferiority, randomised controlled trial. Lancet Oncol. 2014;15:767–74.

    Article  PubMed  Google Scholar 

  11. Van der Pas MHGM, Haglind E, Cuesta MA, Fürst A, Macy AM, Hop WCJ, Bonjer HJ, for the Colorectal cancer Laparoscopic or Open resection II (COLOR II) Study Group. Laparoscopic versus open surgery for rectal cancer (COLOR II): short-term outcomes of a randomized, phase 3 trial. Lancet Oncol. 2013;14:210–8.

    Article  PubMed  Google Scholar 

  12. Bonjer HJ, Deijen CL, Abis GA, et al. for the COLOR II Study Group. A randomized trial of laparoscopic versus open surgery for rectal cancer. N Engl J Med. 2015;372:1324–32.

    Article  CAS  PubMed  Google Scholar 

  13. Fleshman J, Branda M, Sargent DJ, et al. 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. 2015;314:1346–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Stevenson AR, Solomon MJ, Lumley JW, et al. Effect of laparoscopic-assisted resection vs open resection on pathological outcomes in rectal cancer: the ALaCaRT Randomized Clinical Trial. JAMA. 2015;314:1356–63.

    Article  CAS  PubMed  Google Scholar 

  15. Yang Q, Xiu P, Qi X, Yi G, Xu L. Surgical margins and short-term results of laparoscopic total mesorectal excision for low rectal cancer. JSLS. 2013;17:212–8.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Midura EF, Hanseman DJ, Hoehn RS, Davis BR, Abbott DE, Shah SA, Paquette IM. The effect of surgical approach on short-term outcomes in rectal cancer surgery. Surgery. 2015;158:453–9.

    Article  PubMed  Google Scholar 

  17. Nussbaum DP, Speicher PJ, Ganapathi AM, Englum BR, Keenan JE, Mantyh CR, Migaly J. Laparoscopic versus open low anterior resection for rectal cancer: results from the National Cancer Data Base. J Gastrointest Surg. 2015;19:124–32.

    Article  PubMed  Google Scholar 

  18. Rickles AS, Dietz DW, Chang GJ, et al. On Behalf of The Consortium for Optimizing the Treatment of Rectal Cancer (OSTRiCh). Ann Surg. 262:891–8.

  19. Steele SR, Stein SL, Bordeianou LG, Johnson E, Herzig DO, Champagne BJ; American Society of Colon and Rectal Surgeons’ Young Surgeons Committee. The impact of practice environment on laparoscopic colectomy utilization following colorectal residency: a survey of the ASCRS Young Surgeons. Colorectal Dis. 2012;14(3):374–81.

    Article  PubMed  Google Scholar 

  20. Disbrow DE, Pannell SM, Shanker BA, et al. The effect of formal robotic residency training on the adoption of minimally invasive surgery by young colorectal surgeons. J Surg Educ. 2018;75:767–78.

    Article  PubMed  Google Scholar 

  21. Miskovic D, Foster J, Agha A, et al. Standardization of laparoscopic total mesorectal excision for rectal cancer: a structured international expert consensus. Ann Surg. 2015;261:716–22.

    Article  PubMed  Google Scholar 

  22. Van de Velde CJ, Boelens PG, Tanis PJ, et al. Expert reviews of the multidisciplinary consensus conference colon and rectal cancer 2012: science, opinions, and experiences from the experts of surgery. Eur J Surg Oncol. 2014;40:454–68.

    Article  PubMed  Google Scholar 

  23. Schardt C, Adams MB, Owens T, Keitz S, Fontelo P. Utilization of the PICO framework to improve searching PubMed for clinical questions. BMC Med Inform Decis Mak. 2007;7:16. http://dx.doi.org/10.1186/1472-6947-7-1.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol. 2009;62(10):e1–34. https://doi.org/10.1016/j.jclinepi.2009.06.006. Epub 2009 Jul 23.

    Article  PubMed  Google Scholar 

  25. Fueglistaler P, Adamina M, Guller U. Non-inferiority trials in surgical oncology. Ann Surg Oncol. 2007;14(5):1532–9. https://doi.org/10.1245/s10434-006-9295-2.

    Article  PubMed  Google Scholar 

  26. Lujan J, Valero G, Biondo S, Espin E, Parrilla P, Ortiz H. Laparoscopic versus open surgery for rectal cancer: results of a prospective multicentre analysis of 4,970 patients. Surg Endosc. 2013;27:295–302.

    Article  CAS  PubMed  Google Scholar 

  27. Penninckx F, Kartheuser A, Van de Statd J, et al; PROCARE. Outcome following laparoscopic and open total mesorectal excision for rectal cancer. Br J Surg. 2013;100:1368–75.

    Article  CAS  PubMed  Google Scholar 

  28. Li S, Jiang F, Tu J, Zheng X. Long-term oncologic outcomes of laparoscopic versus open surgery for middle and lower rectal cancer. PLoS ONE. 2015;10(9):e0135884. https://doi.org/10.1371/journal.pone.0135884. eCollection 2015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Biondo S, Ortiz H, Lujan J, et al. Quality of mesorectum after laparoscopic resection for rectal cancer: results of an audited teaching programme in Spain. Colorectal Dis. 2010;12:24–32.

    Article  CAS  PubMed  Google Scholar 

  30. Feliciotti F, Guerrieri M, Paganini AM, et al. Long-term results of laparoscopic versus open resections for rectal cancer for 124 unselected patients. Surg Endosc. 2003;17:1530–5.

    Article  CAS  PubMed  Google Scholar 

  31. Lelong B, Bege T, Esterni B, et al. Short-term outcome after laparoscopic or open restorative excision for rectal cancer: a comparative cohort study. Dis Colon Rectum. 2007;50:176–83.

    Article  PubMed  Google Scholar 

  32. Staudacher C, Vignali A, Saverio DP, Elena O, Andrea T. Laparoscopic vs. open total mesorectal excision in unselected patients with rectal cancer: impact on early outcome. Dis Colon Rectum. 2007;50:1324–31.

    Article  PubMed  Google Scholar 

  33. Strolein MA, Grützner KU, Jauch KW, Heiss MM. Comparison of laparoscopic vs. open access surgery in patients with rectal cancer: a prospective analysis. Dis Colon Rectum. 2008;51:385–91.

    Article  Google Scholar 

  34. Wang A, Zhang XM, Liang JW, Zeng WG, Zhou ZX. Evaluation of short-term outcomes after laparoscopically assisted abdominoperineal resection for low rectal cancer. ANZ J Surg. 2014;84:842–6.

    Article  PubMed  Google Scholar 

  35. Gezen C, Altuntas YE, Kement M, Aksakal N, Okkabaz N, Vural S, Oncel M. Laparoscopic and conventional resections for low rectal cancers: a retrospective analysis on perioperative outcomes, sphincter preservation, and oncologic results. J Laparoendosc Adv Surg Tech A. 2012;22:625–30.

    Article  PubMed  Google Scholar 

  36. Spelcher PJ, Englum BR, Ganapathi AM, Nussbaum DP, Mantyh CR, Migaly J. Robotic low anterior resection for rectal cancer: a national perspective on short-term oncologic outcomes. Ann Surg. 2015;262:1040–5.

    Article  Google Scholar 

  37. Ding KF, Chen R, Zhang JL, et al. Laparoscopic surgery for the curative treatment of rectal cancer: results of a Chinese three-center case-control study. Surg Endosc. 2009;23:854–61.

    Article  PubMed  Google Scholar 

  38. McKay GD, Morgan MJ, Wong SK, et al; South Western Sydney Colorectal Tumor Group. Improved short-term outcomes of laparoscopic versus open resection for colon and rectal cancer in an area health service: a multicenter study. Dis Colon Rectum. 2012;55:42–50.

    Article  PubMed  Google Scholar 

  39. Saklani AP, Lim DR, Hur H, Min BS, Baik SH, Lee KY, Kim NK. Robotic versus laparoscopic surgery for mid-low rectal cancer after neoadjuvant chemoradiation therapy: comparison of oncologic outcomes. Int J Colorectal Dis. 2013;28:1689–98.

    Article  PubMed  Google Scholar 

  40. Zhou ZX, Zhao LY, Lin T, et al. Long-term oncologic outcomes of laparoscopic vs open surgery for stages II and III rectal cancer: a retrospective cohort study. World J Gastroenterol. 2015;21:5505–12.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Keller DS, Khorgami Z, Swenddeis B, Champagne BJ, Reynolds HL Jr, Stein SL, Delaney CP. Laparoscopic and converted approaches to rectal cancer resection have superior long-term outcomes: a comparative study by operative approach. Surg Endosc. 2014;28:1940–8.

    Article  PubMed  Google Scholar 

  42. Kellokumpu IH, Kairaluoma MI, Nuorva KP, Kautiainen HJ, Jantunen IT. Short- and long-term outcome following laparoscopic versus open resection for carcinoma of the rectum in the multimodal setting. Dis Colon Rectum. 2012;55:854–63.

    Article  PubMed  Google Scholar 

  43. Baik SH, Gincherman M, Mutch MG, Birnbaum EH, Fleshman JW. Laparoscopic vs open resection for patients with rectal cancer: comparison of perioperative outcomes and long-term survival. Dis Colon Rectum. 2011;54:6–14.

    Article  PubMed  Google Scholar 

  44. Cho MS, Kim CW, Baek SJ, et al. Minimally invasive versus open total mesorectal excision for rectal cancer: long-term results from a case-matched study of 633 patients. Surgery. 2015;157:1121–9.

    Article  PubMed  Google Scholar 

  45. Lee SD, Park SC, Park JW, Kim DY, Choi HS, Oh JH. Laparoscopic versus open surgery for stage I rectal cancer: long-term oncologic outcomes. World J Surg. 2013;37:646–51.

    Article  PubMed  Google Scholar 

  46. Sara S, Poncet G, Voirin D, Laverriere MH, Anglade D, Faucheron JL. Can adequate lymphadenectomy be obtained by laparoscopic resection in rectal cancer? Results of a case-control study in 200 patients. J Gastrointest Surg. 2010;14:1244–7.

    Article  PubMed  Google Scholar 

  47. Park JS, Choi GS, Lim KH, Jang YS, Jun SH. S052: a comparison of robot-assisted, laparoscopic, and open surgery in the treatment of rectal cancer. Surg Endosc. 2011;25:240–8.

    Article  PubMed  Google Scholar 

  48. Hu JJ, Liang JW, Wang Z, Zhang XM, Zhou HT, Hou HR, Zhou ZX. Short-term outcomes of laparoscopically assisted surgery for rectal cancer following neoadjuvant chemoradiotherapy: a single-center experience. J Surg Res. 2014;187:438–44.

    Article  PubMed  Google Scholar 

  49. Li Z, Ying X, Shen Y, Ye P, Pan W, Chen H. Laparoscopic versus open surgery for rectal cancer: a clinical comparative study. J Int Med Res. 2012;40:1599–607.

    Article  CAS  PubMed  Google Scholar 

  50. Ghezzi TL, Luca F, Valvo M, Corleta OC, Zuccaro M, Cenciarelli S, Biffi R. Robotic versus open total mesorectal excision for rectal cancer: comparative study of short and long-term outcomes. Eur J Surg Oncol. 2014;40:1072–9.

    Article  CAS  PubMed  Google Scholar 

  51. Boutrous M, Hippalgaonkar N, Silva E, Allende D, Wexner SD, Berho M. Laparoscopic resection of rectal cancer results in higher lymph node yield and better short-term outcomes than open surgery: a large single-center study. Dis Colon Rectum. 2013;56:679–88.

    Article  Google Scholar 

  52. Dural AC, Keskin M, Balik E, et al. The role of the laparoscopy on circumferential resection margin positivity in patients with rectal cancer: long-term outcomes at a single high-volume institution. Surg Laparosc Endosc Percutan Tech. 2015;25:129–37.

    Article  PubMed  Google Scholar 

  53. Schiphorst AH, Doeksen A, Hamaker ME, Zimmerman DD, Pronk A. Short-term follow-up after laparoscopic versus conventional total mesorectal excision for low rectal cancer in a large teaching hospital. Int J Colorectal Dis. 2014;29:117–25.

    Article  CAS  PubMed  Google Scholar 

  54. Wang YW, Huang LY, Song, CL, et al. Laparoscopic vs open abdominoperineal resection in the multimodality management of low rectal cancers. World J Gastroenterol. 2015;21:10174–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Law WL, Poon JT, Fan JK, Lo SH. Comparison of outcome of open and laparoscopic resection for stage II and stage III rectal cancer. Ann Surg Oncol. 2009;16:1488–93.

    Article  PubMed  Google Scholar 

  56. Laurent C, Paumet T, Leblanc F, Denost Q, Rullier E. Intersphincteric resection for low rectal cancer: laparoscopic vs open surgery approach. Colorectal Dis. 2012;14:35–41.

    Article  CAS  PubMed  Google Scholar 

  57. Heald RJ, Husband EM, Ryall RD. The mesorectum in rectal cancer surgery: the clue to pelvic recurrence? Br J Surg. 1982;82:613–6.

    Article  Google Scholar 

  58. Battersby NJ, How P, Moran B, et al; on behalf of the MERCURY II Study Group. Prospective validation of a low rectal cancer magnetic resonance imaging staging system and development of a local recurrence risk stratification model. The MERCURY II Study. Ann Surg. 2016;263:751–60.

    Article  PubMed  Google Scholar 

  59. Nagtegaal ID, Quirke P. What is the role of the circumferential margin in the modern treatment of rectal cancer. J Clin Oncol. 2008;26:303–12.

    Article  PubMed  Google Scholar 

  60. Jayne D, Pigazzi A, Marshall H, et al. Effect of robotic-assisted vs conventional laparoscopic surgery on risk of conversion to open laparotomy among patients undergoing resection for rectal cancer: The ROLARR Randomized Clinical Trial. JAMA. 2017;318:1569–80.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Delivering high-quality cancer care: charting a new course for a system in crisis. Committee on Improving the Quality of Cancer Care: Addressing the challenges of an aging population; Board on Health Care Services; Institute of Medicine; Levit L, Balogh E, Nass S, Ganz PA, eds. Washington (DC); National Academies Press (US); 2013 Dec.

  62. Wexner SD, Berho ME. The rationale for and reality of the New National Accreditation Program for Rectal Cancer. Dis Colon Rectum. 2017;60:595–602.

    Article  PubMed  Google Scholar 

  63. https://www.facs.org/quality-programs/cancer/naprc.

  64. Deijen CL, Velthius S, Tsai A, et al. COLOR III: a multicentre randomised clinical trial comparing transanal TME versus laparoscopic TME for mid and low rectal cancer. Surg Endosc. 2016;30:3210–5.

    Article  PubMed  Google Scholar 

Download references

Funding Information

No grant support or other funds were received for this work.

Disclosures

Dr. Cleary has received honoraria from Intuitive Surgical, Inc. for educational speaking. He has received research funding from Blue Cross Blue Shield of Michigan. Dr. Morris has no conflict of interest to disclose. Dr. Chang is a consultant to Johnson and Johnson and MORE Health. He has received research funding from Agendia. Dr. Halverson has no conflict of interest to disclose.

Author information

Authors and Affiliations

  1. Division of Colon and Rectal Surgery, St Joseph Mercy Hospital Ann Arbor, Ann Arbor, MI, USA

    Robert K. Cleary MD

  2. Section of Colon and Rectal Surgery, Stanford University Medical Center, Stanford, CA, USA

    Arden M. Morris MD

  3. Department of Surgical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA

    George J. Chang MD

  4. Division of Colon and Rectal Surgery, Northwestern University Feinberg School of Medicine, Chicago, IL, USA

    Amy L. Halverson MD

Authors
  1. Robert K. Cleary MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Arden M. Morris MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. George J. Chang MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Amy L. Halverson MD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Robert K. Cleary MD.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cleary, R.K., Morris, A.M., Chang, G.J. et al. Controversies in Surgical Oncology: Does the Minimally Invasive Approach for Rectal Cancer Provide Equivalent Oncologic Outcomes Compared with the Open Approach?. Ann Surg Oncol 25, 3587–3595 (2018). https://doi.org/10.1245/s10434-018-6740-y

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1245/s10434-018-6740-y

Search

Navigation