Short- and Long-Term Oncological Outcome After Rectal Cancer Surgery: a Systematic Review and Meta-Analysis Comparing Open Versus Laparoscopic Rectal Cancer Surgery

  • Henrik Nienhüser
  • Patrick Heger
  • Robin Schmitz
  • Yakup Kulu
  • Markus K. Diener
  • Johannes Klose
  • Martin Schneider
  • Beat P. Müller-Stich
  • Alexis Ulrich
  • Markus W. Büchler
  • Andre L. Mihaljevic
  • Thomas Schmidt
Original Article
  • 97 Downloads

Abstract

Background

While several trials have compared laparoscopic to open surgery for colon cancer showing similar oncological results, oncological quality of laparoscopic versus open rectal resection is not well investigated.

Methods

A systematic literature search for randomized controlled trials was conducted in MEDLINE, the Cochrane Library, and Embase. Qualitative and quantitative meta-analyses of short-term (rate of complete resections, number of harvested lymph nodes, circumferential resection margin positivity) and long-term (recurrence, disease-free and overall survival) oncologic results were conducted.

Results

Fourteen randomized controlled trials were identified including 3528 patients. Patients in the open resection group had significantly more complete resections (OR 0.70; 95% CI 0.51–0.97; p = 0.03) and a higher number of resected lymph nodes (mean difference − 0.92; 95% CI − 1.08 to 0.75; p < 0.001). No differences were detected in the frequency of positive circumferential resection margins (OR 0.82; 95% CI 0.62–1.10; p = 0.18). Furthermore, no significant differences of long-term oncologic outcome parameters after 5 years including locoregional recurrence (OR 0.95; 95% CI 0.44–2.05; p = 0.89), disease-free survival (OR 1.16; 95% CI 0.84–1.58; p = 0.36), and overall survival (OR 1.04; 95% CI 0.76–1.41; p = 0.82) were found. Most trials exhibited a relevant risk of bias and several studies provided no information on the surgical expertise of the participating surgeons.

Conclusion

Differences in oncologic outcome between laparoscopic and open rectal surgery for rectal cancer were detected for the complete resection rate and the number of resected lymph nodes in favor of the open approach. No statistically significant differences were found in oncologic long-term outcome parameters.

Keywords

Rectal cancer Laparoscopic surgery Systematic review Meta-analysis 

Notes

Authors’ Contribution

HN, PH, RS, BPM, ALM, and TS are responsible for the conception and design of the study. HN, PH, RS, ALM, and TS performed the acquisition and analysis of the data and drafted the manuscript. YK, MKD, JK, MS, BPM, AU, and MWB offered substantial contributions to the interpretation of the data and critically revised the manuscript. All authors gave their final approval of this version of the manuscript and are accountable for all aspects of the work.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

11605_2018_3738_MOESM1_ESM.docx (67 kb)
ESM 1 (DOCX 67 kb)

References

  1. 1.
    Siegel, R., C. Desantis, and A. Jemal, Colorectal cancer statistics, 2014. CA Cancer J Clin, 2014. 64(2): p. 104–17.CrossRefPubMedGoogle Scholar
  2. 2.
    Edwards, B.K., et al., Annual report to the nation on the status of cancer, 1975-2006, featuring colorectal cancer trends and impact of interventions (risk factors, screening, and treatment) to reduce future rates. Cancer, 2010. 116(3): p. 544–73.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Heald, R.J., E.M. Husband, and R.D. Ryall, The mesorectum in rectal cancer surgery—the clue to pelvic recurrence? Br J Surg, 1982. 69(10): p. 613–6.CrossRefPubMedGoogle Scholar
  4. 4.
    Jacobs, M., J.C. Verdeja, and H.S. Goldstein, Minimally invasive colon resection (laparoscopic colectomy). Surg Laparosc Endosc, 1991. 1(3): p. 144–50.PubMedGoogle Scholar
  5. 5.
    van der Pas, M.H., et al., Laparoscopic versus open surgery for rectal cancer (COLOR II): short-term outcomes of a randomised, phase 3 trial. Lancet Oncol, 2013. 14(3): p. 210–8.CrossRefPubMedGoogle Scholar
  6. 6.
    Stead, M.L., et al., Assessing the relative costs of standard open surgery and laparoscopic surgery in colorectal cancer in a randomised controlled trial in the United Kingdom. Crit Rev Oncol Hematol, 2000. 33(2): p. 99–103.CrossRefPubMedGoogle Scholar
  7. 7.
    Guillou, P.J., 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): p. 1718–26.CrossRefPubMedGoogle Scholar
  8. 8.
    Theophilus, M., C. Platell, and K. Spilsbury, Long-term survival following laparoscopic and open colectomy for colon cancer: a meta-analysis of randomized controlled trials. Colorectal Dis, 2014. 16(3): p. O75–81.CrossRefPubMedGoogle Scholar
  9. 9.
    Wang, C.L., G. Qu, and H.W. Xu, The short- and long-term outcomes of laparoscopic versus open surgery for colorectal cancer: a meta-analysis. Int J Colorectal Dis, 2014. 29(3): p. 309–20.CrossRefPubMedGoogle Scholar
  10. 10.
    Di, B., et al., Laparoscopic versus open surgery for colon cancer: a meta-analysis of 5-year follow-up outcomes. Surg Oncol, 2013. 22(3): p. e39–43.CrossRefPubMedGoogle Scholar
  11. 11.
    Kuhry, E., et al., Long-term outcome of laparoscopic surgery for colorectal cancer: a cochrane systematic review of randomised controlled trials. Cancer Treat Rev, 2008. 34(6): p. 498–504.CrossRefPubMedGoogle Scholar
  12. 12.
    Vennix, S., et al., Laparoscopic versus open total mesorectal excision for rectal cancer. Cochrane Database Syst Rev, 2014(4): p. Cd005200.Google Scholar
  13. 13.
    Biondi, A., et al., Laparoscopic vs. open approach for colorectal cancer: evolution over time of minimal invasive surgery. BMC Surg, 2013. 13 Suppl 2: p. S12.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Panic, N., et al., 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, 2013. 8(12): p. e83138.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Higgins, J.P., et al., The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. Bmj, 2011. 343: p. d5928.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Bonjer, H.J., C.L. Deijen, and E. Haglind, A Randomized Trial of Laparoscopic versus Open Surgery for Rectal Cancer. N Engl J Med, 2015. 373(2): p. 194.PubMedGoogle Scholar
  17. 17.
    Jayne, D.G., et al., 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(11): p. 1638–45.CrossRefPubMedGoogle Scholar
  18. 18.
    Jayne, D.G., et al., Randomized trial of laparoscopic-assisted resection of colorectal carcinoma: 3-year results of the UK MRC CLASICC Trial Group. J Clin Oncol, 2007. 25(21): p. 3061–8.CrossRefPubMedGoogle Scholar
  19. 19.
    Green, B.L., et al., Long-term follow-up of the Medical Research Council CLASICC trial of conventional versus laparoscopically assisted resection in colorectal cancer. Br J Surg, 2013. 100(1): p. 75–82.CrossRefPubMedGoogle Scholar
  20. 20.
    Kang, S.B., et al., Open versus laparoscopic surgery for mid or low rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): short-term outcomes of an open-label randomised controlled trial. Lancet Oncol, 2010. 11(7): p. 637–45.CrossRefPubMedGoogle Scholar
  21. 21.
    Jeong, S.Y., 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(7): p. 767–74.CrossRefPubMedGoogle Scholar
  22. 22.
    Leung, K.L., et al., Laparoscopic resection of rectosigmoid carcinoma: prospective randomised trial. Lancet, 2004. 363(9416): p. 1187–92.CrossRefPubMedGoogle Scholar
  23. 23.
    Ng, S.S., et al., Long-term morbidity and oncologic outcomes of laparoscopic-assisted anterior resection for upper rectal cancer: ten-year results of a prospective, randomized trial. Dis Colon Rectum, 2009. 52(4): p. 558–66.CrossRefPubMedGoogle Scholar
  24. 24.
    Braga, M., et al., Laparoscopic resection in rectal cancer patients: outcome and cost-benefit analysis. Dis Colon Rectum, 2007. 50(4): p. 464–71.CrossRefPubMedGoogle Scholar
  25. 25.
    Fleshman, J., 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(13): p. 1346–55.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Liu, F.L., et al., Hand-assisted laparoscopic surgery versus the open approach in curative resection of rectal cancer. J Int Med Res, 2010. 38(3): p. 916–22.CrossRefPubMedGoogle Scholar
  27. 27.
    Lujan, J., et al., Randomized clinical trial comparing laparoscopic and open surgery in patients with rectal cancer. Br J Surg, 2009. 96(9): p. 982–9.CrossRefPubMedGoogle Scholar
  28. 28.
    Ng, S.S., et al., Laparoscopic-assisted versus open total mesorectal excision with anal sphincter preservation for mid and low rectal cancer: a prospective, randomized trial. Surg Endosc, 2014. 28(1): p. 297–306.CrossRefPubMedGoogle Scholar
  29. 29.
    Pechlivanides, G., et al., Lymph node clearance after total mesorectal excision for rectal cancer: laparoscopic versus open approach. Dig Dis, 2007. 25(1): p. 94–9.CrossRefPubMedGoogle Scholar
  30. 30.
    Stevenson, A.R., et al., Effect of Laparoscopic-Assisted Resection vs Open Resection on Pathological Outcomes in Rectal Cancer: The ALaCaRT Randomized Clinical Trial. JAMA, 2015. 314(13): p. 1356–63.CrossRefPubMedGoogle Scholar
  31. 31.
    Zhou, Z.G., et al., Laparoscopic versus open total mesorectal excision with anal sphincter preservation for low rectal cancer. Surg Endosc, 2004. 18(8): p. 1211–5.CrossRefPubMedGoogle Scholar
  32. 32.
    Liang, X., 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(5): p. 381–5.CrossRefPubMedGoogle Scholar
  33. 33.
    Kennedy, R.H., et al., Multicenter randomized controlled trial of conventional versus laparoscopic surgery for colorectal cancer within an enhanced recovery programme: EnROL. J Clin Oncol, 2014. 32(17): p. 1804–11.CrossRefPubMedGoogle Scholar
  34. 34.
    Strobel, O. and M.W. Buchler, The problem of the poor control arm in surgical randomized controlled trials. Br J Surg, 2013. 100(2): p. 172–3.CrossRefPubMedGoogle Scholar
  35. 35.
    Bege, T., et al., The learning curve for the laparoscopic approach to conservative mesorectal excision for rectal cancer: lessons drawn from a single institution’s experience. Ann Surg, 2010. 251(2): p. 249–53.CrossRefPubMedGoogle Scholar
  36. 36.
    Kayano, H., et al., Evaluation of the learning curve in laparoscopic low anterior resection for rectal cancer. Surg Endosc, 2011. 25(9): p. 2972–9.CrossRefPubMedGoogle Scholar
  37. 37.
    Son, G.M., et al., Multidimensional analysis of the learning curve for laparoscopic rectal cancer surgery. J Laparoendosc Adv Surg Tech A, 2010. 20(7): p. 609–17.CrossRefPubMedGoogle Scholar
  38. 38.
    Leibold, T., et al., Prognostic implications of the distribution of lymph node metastases in rectal cancer after neoadjuvant chemoradiotherapy. J Clin Oncol, 2008. 26(13): p. 2106–11.CrossRefPubMedGoogle Scholar
  39. 39.
    Kim, C.H., et al., Learning curve of laparoscopic low anterior resection in terms of local recurrence. J Surg Oncol, 2014. 110(8): p. 989–96.CrossRefPubMedGoogle Scholar
  40. 40.
    Sauer, R., et al., Adjuvant vs. neoadjuvant radiochemotherapy for locally advanced rectal cancer: the German trial CAO/ARO/AIO-94. Colorectal Dis, 2003. 5(5): p. 406–15.CrossRefPubMedGoogle Scholar

Copyright information

© The Society for Surgery of the Alimentary Tract 2018

Authors and Affiliations

  • Henrik Nienhüser
    • 1
  • Patrick Heger
    • 1
    • 2
  • Robin Schmitz
    • 1
    • 3
  • Yakup Kulu
    • 1
  • Markus K. Diener
    • 1
    • 2
  • Johannes Klose
    • 1
  • Martin Schneider
    • 1
  • Beat P. Müller-Stich
    • 1
  • Alexis Ulrich
    • 1
  • Markus W. Büchler
    • 1
  • Andre L. Mihaljevic
    • 1
    • 2
  • Thomas Schmidt
    • 1
  1. 1.Department of General, Visceral and Transplant SurgeryUniversity of HeidelbergHeidelbergGermany
  2. 2.Study Center of the German Surgical Society (SDGC)University of HeidelbergHeidelbergGermany
  3. 3.Department of SurgeryDuke University Medical CenterDurhamUSA

Personalised recommendations