Skip to main content

Advertisement

SpringerLink
Log in

Effects of surgical approach on short- and long-term outcomes in early-stage rectal cancer: a multicenter, propensity score-weighted cohort study

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

Randomized controlled trials have been unable to demonstrate noninferiority of minimally invasive surgery for rectal cancer. The aim of this study was to assess oncologic resection success, short- and long-term morbidity, and overall survival by operative approach in a homogenous early-stage rectal cancer cohort.

Methods

This is a multicenter, propensity score-weighted cohort study utilizing deidentified data from the National Cancer Database. Individuals who underwent a formal proctectomy for early-stage rectal cancer (T1-2, N0, M0) from 2010 to 2015 were included. The primary outcome was a composite variable indicating successful oncologic resection stratified by operative approach, defined as negative margins with at least 12 lymph nodes evaluated.

Results

Among 3649 proctectomies for rectal adenocarcinoma, 1660 (45%) were approached open, 1461 (40%) laparoscopically, and 528 (15%) robotically. After propensity score weighting, compared to open approach, there were no differences in odds of successful oncologic resection (ORadj = 1.07, 95% CI 0.9, 1.28 and ORadj = 1.28, 95% CI 0.97, 1.7). Open approach was associated with longer mean (± SD) length of stay compared to laparoscopic (7.7 ± 0.18 vs. 6.5 ± 0.25 days, p < 0.001) and robotic (7.7 ± 0.18 vs. 6.3 ± 0.35 days, p < 0.001) approaches. In regard to 90-day mortality, compared to open approach, laparoscopic (ORadj = 0.56, 95% CI 0.36, 0.88) and robotic (ORadj = 0.45, 95% CI 0.22, 0.94) approaches were associated with a reduced odd of 90-day mortality. This mortality benefit persists in the long-term for laparoscopic approach (p = 0.003).

Conclusion

For individuals with early-stage rectal cancer treated with proctectomy, successful oncologic resection can be achieved irrespective of technical approach. Minimally invasive approaches provide short-term reduction in morbidity. Surgical approach must be tailored to each patient based on surgeon experience and judgement in collaboration with a multi-disciplinary team.

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
Fig. 2

Similar content being viewed by others

References

  1. Siegel RL, Miller KD, Jemal A (2019) Cancer statistics. CA Cancer J Clin 69:7–34. https://doi.org/10.3322/caac.21551

    Article  PubMed  Google Scholar 

  2. Konstantinidis IT, Ituarte P, Woo Y, Warner SG, Melstrom K, Kim J, Singh G, Lee B, Fong Y, Melstrom LG (2019) Trends and outcomes of robotic surgery for gastrointestinal (GI) cancers in the USA: maintaining perioperative and oncologic safety. Surg Endosc. https://doi.org/10.1007/s00464-019-07284-x

    Article  PubMed  PubMed Central  Google Scholar 

  3. Jayne D, Pigazzi A, Marshall H, Croft J, Corrigan N, Copeland J, Quirke P, West N, Rautio T, Thomassen N, Tilney H, Gudgeon M, Pietro BP, Edlin R, Hulme C, Brown J (2017) 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 - J Am Med Assoc 318:1569–1580. https://doi.org/10.1001/jama.2017.7219

    Article  Google Scholar 

  4. Kim MJ, Park SC, Park JW, Chang HJ, Kim DY, Nam B-H, Sohn DK, Oh JH (2018) Robot-assisted versus laparoscopic surgery for rectal cancer: A Phase II open label prospective randomized controlled trial. Ann Surg 267:243–251. https://doi.org/10.1097/SLA.0000000000002321

    Article  PubMed  Google Scholar 

  5. van der Pas MH, Haglind E, Cuesta MA, Fürst 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. https://doi.org/10.1016/S1470-2045(13)70016-0

    Article  PubMed  Google Scholar 

  6. Stevenson ARL, Solomon MJ, Brown CSB, Lumley JW, Hewett P, Clouston AD, Gebski VJ, Wilson K, Hague W, Simes J, Australasian Gastro-Intestinal Trials Group (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. https://doi.org/10.1097/SLA.0000000000003021

    Article  Google Scholar 

  7. Fleshman J, Branda ME, Sargent DJ, Boller AM, George VV, Abbas MA, Peters WR, Maun DC, Chang GJ, Herline A, Fichera A, Mutch MG, Wexner SD, Whiteford MH, Marks J, Birnbaum E, Margolin DA, Larson DW, Marcello PW, Posner MC, Read TE, Monson JRT, Wren SM, Pisters PWT, Nelson H (2019) Disease-free survival and local recurrence for laparoscopic resection compared with open resection of stage II to III rectal cancer: follow-up results of the ACOSOG Z6051 randomized controlled trial. Ann Surg 269:589–595. https://doi.org/10.1097/SLA.0000000000003002

    Article  PubMed  Google Scholar 

  8. Martínez-Pérez A, Carra MC, Brunetti F, De’Angelis N, (2017) Pathologic outcomes of laparoscopic vs open mesorectal excision for rectal cancer: A systematic review and meta-analysis. JAMA Surg 152:e165665

    Article  Google Scholar 

  9. Prete FP, Pezzolla A, Prete F, Testini M, Marzaioli R, Patriti A, Jimenez-Rodriguez RM, Gurrado A, Strippoli GFM (2018) Robotic versus laparoscopic minimally invasive surgery for rectal cancer: a systematic review and meta-analysis of randomized controlled trials. Ann Surg 267:1034–1046. https://doi.org/10.1097/SLA.0000000000002523

    Article  PubMed  Google Scholar 

  10. Kolarich A, George TJ, Hughes SJ, Delitto D, Allegra CJ, Hall WA, Chang GJ, Tan SA, Shaw CM, Iqbal A (2018) Rectal cancer patients younger than 50 years lack a survival benefit from NCCN guideline–directed treatment for stage II and III disease. Cancer 124:3510–3519. https://doi.org/10.1002/cncr.31527

    Article  PubMed  Google Scholar 

  11. Leo E, Belli F, Miceli R, Mariani L, Gallino G, Battaglia L, Vannelli A, Andreola S (2009) Distal clearance margin of 1 cm or less: a safe distance in lower rectum cancer surgery. Int J Colorectal Dis 24:317–322. https://doi.org/10.1007/s00384-008-0604-z

    Article  PubMed  Google Scholar 

  12. Grosek J, Velenik V, Edhemovic I, Omejc M (2017) 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. https://doi.org/10.1515/raon-2016-0030

    Article  PubMed  Google Scholar 

  13. Fitzgerald TL, Brinkley J, Zervos EE (2011) Pushing the envelope beyond a centimeter in rectal cancer: oncologic implications of close, but negative margins. J Am Coll Surg 213:589–595. https://doi.org/10.1016/j.jamcollsurg.2011.07.020

    Article  PubMed  Google Scholar 

  14. Tepper JE, O’Connell MJ, Niedzwiecki D, Hollis D, Compton C, Benson AB, Cummings B, Gunderson L, Macdonald JS, Mayer RJ (2001) Impact of number of nodes retrieved on outcome in patients with rectal cancer. J Clin Oncol Off J Am Soc Clin Oncol 19:157–163. https://doi.org/10.1200/JCO.2001.19.1.157

    Article  CAS  Google Scholar 

  15. Nagtegaal ID, Quirke P (2008) What is the role for the circumferential margin in the modern treatment of rectal cancer? J Clin Oncol Off J Am Soc Clin Oncol 26:303–312. https://doi.org/10.1200/JCO.2007.12.7027

    Article  Google Scholar 

  16. Friedman J (2001) Greedy function approximation: a gradient boosting machine. Ann Stat. https://doi.org/10.1214/aos/1013203451

    Article  Google Scholar 

  17. Efron B, Hastie T, Johnstone I (2004) Least angle regression. Ann Stat. https://doi.org/10.1214/009053604000000067

    Article  Google Scholar 

  18. McCaffrey D, Ridgeway G, Morral A (2004) Propensity score estimation with boosted regression for evaluating causal effects in observational studies. Psychol Methods 9(4):403–425

    Article  Google Scholar 

  19. McCaffrey DF, Griffin BA, Almirall D, Slaughter ME, Ramchand R, Burgette LF (2013) A tutorial on propensity score estimation for multiple treatments using generalized boosted models. Stat Med 32:3388–3414. https://doi.org/10.1002/sim.5753

    Article  PubMed  PubMed Central  Google Scholar 

  20. Ridgeway G, McCaffrey D, Morral A, Burgette L, Ann Griffin B (2017) Toolkit for Weighting and Analysis of Nonequivalent Groups: A tutorial for the twang package

  21. von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP, Initiative STROBE (2014) The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement: guidelines for reporting observational studies. Int J Surg Lond Engl 12:1495–1499. https://doi.org/10.1016/j.ijsu.2014.07.013

    Article  Google Scholar 

  22. Jeong S-Y, Park JW, Nam BH, Kim S, Kang S-B, Lim S-B, Choi HS, Kim D-W, Chang HJ, Kim DY, Jung KH, Kim T-Y, Kang GH, Chie EK, Kim SY, Sohn DK, Kim D-H, Kim J-S, Lee HS, Kim JH, Oh JH (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, randomised controlled trial. Lancet Oncol 15:767–774. https://doi.org/10.1016/S1470-2045(14)70205-0

    Article  PubMed  Google Scholar 

  23. Fleshman J, Branda M, Sargent DJ, Boller AM, George V, Abbas M, Peters WR, 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. https://doi.org/10.1001/jama.2015.10529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Stevenson ARL, Solomon MJ, Lumley JW, Hewett P, Clouston AD, Gebski VJ, Davies L, Wilson K, Hague W, Simes J, ALaCaRT Investigators, (2015) Effect of laparoscopic-assisted resection vs open resection on pathological outcomes in rectal cancer: The ALaCaRT randomized clinical trial. JAMA 314:1356–1363. https://doi.org/10.1001/jama.2015.12009

    Article  CAS  PubMed  Google Scholar 

  25. Vennix S, Pelzers L, Bouvy N, Beets GL, Pierie J-P, Wiggers T, Breukink S (2014) Laparoscopic versus open total mesorectal excision for rectal cancer. In: Breukink S (ed) Cochrane Database of Systematic Reviews. John Wiley & Sons Ltd, Chichester UK, p CD05200

    Google Scholar 

  26. Quintana JM, Anton-Ladislao A, Lázaro S, Gonzalez N, Bare M, de Larrea NF, Redondo M, Briones E, Escobar A, Sarasqueta C, Garcia-Gutierrez S, Group for the R-C (2017) Outcomes of open versus laparoscopic surgery in patients with rectal cancer. Int J Colorectal Dis. https://doi.org/10.1007/s00384-017-2925-2

    Article  Google Scholar 

  27. Kang S-B, Park JW, Jeong S-Y, Nam BH, Choi HS, Kim D-W, Lim S-B, Lee T-G, Kim DY, Kim J-S, Chang HJ, Lee H-S, Kim SY, Jung KH, Hong YS, Kim JH, Sohn DK, Kim D-H, 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 randomised controlled trial. Lancet Oncol 11:637–645. https://doi.org/10.1016/S1470-2045(10)70131-5

    Article  PubMed  Google Scholar 

  28. Trastulli S, Farinella E, Cirocchi R, Cavaliere D, Avenia N, Sciannameo F, Gullà N, Noya G, Boselli C (2012) Robotic resection compared with laparoscopic rectal resection for cancer: systematic review and meta-analysis of short-term outcome. Colorectal Dis 14:e134–e156. https://doi.org/10.1111/j.1463-1318.2011.02907.x

    Article  CAS  PubMed  Google Scholar 

  29. Xiong B, Ma L, Huang W, Zhao Q, Cheng Y, Liu J (2015) Robotic versus laparoscopic total mesorectal excision for rectal cancer: a Meta-analysis of eight studies. J Gastrointest Surg 19:516–526. https://doi.org/10.1007/s11605-014-2697-8

    Article  PubMed  Google Scholar 

  30. Prete FP, Pezzolla A, Prete F, Testini M, Marzaioli R, Patriti A, Jimenez-Rodriguez RM, Gurrado A, Strippoli GFM (2017) Robotic versus laparoscopic minimally invasive surgery for rectal cancer. Ann Surg. https://doi.org/10.1097/SLA.0000000000002523

    Article  Google Scholar 

  31. Allaix ME, Furnée E, Esposito L, Mistrangelo M, Rebecchi F, Arezzo A, Morino M (2018) Analysis of early and long-term oncologic outcomes after converted laparoscopic resection compared to primary open surgery for rectal cancer. World J Surg 42:3405–3414. https://doi.org/10.1007/s00268-018-4614-x

    Article  PubMed  Google Scholar 

  32. Boffa DJ, Rosen JE, Mallin K, Loomis A, Gay G, Palis B, Thoburn K, Gress D, McKellar DP, Shulman LN, Facktor MA, Winchester DP (2017) Using the national cancer database for outcomes research a review. JAMA Oncol 3:1722–1728. https://doi.org/10.1001/jamaoncol.2016.6905

    Article  PubMed  Google Scholar 

  33. Oxford Centre for Evidence-based Medicine - Levels of Evidence (March 2009) - CEBM. https://www.cebm.net/2009/06/oxford-centre-evidence-based-medicine-levels-evidence-march-2009/. Accessed 21 Dec 2018

Download references

Funding

There were no sources of funding for this research.

Author information

Authors and Affiliations

  1. Department of Surgery, Division of Colorectal Surgery, University Hospitals RISES: Research in Surgical Outcomes and Effectiveness, 11100 Euclid Ave, Cleveland, OH, 44106, USA

    William C. Kethman, Katherine E. Bingmer, Asya Ofshteyn, Ronald Charles, Sharon L. Stein, David Dietz & Emily Steinhagen

Authors
  1. William C. Kethman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katherine E. Bingmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Asya Ofshteyn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ronald Charles
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sharon L. Stein
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. David Dietz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Emily Steinhagen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors substantially contributed to the conception of the manuscript. Dr. Kethman acquired and analyzed the data and Drs. Kethman, Dietz, Stein, and Steinhagen aided in the interpretation of the data and analysis. Dr. Kethman was responsible for drafting initial drafts of the manuscript and Drs. Bingmer, Ofshteyn, Charles, Stein, Dietz, and Steinhagen contributed to critically revising important intellectual content. All authors gave final approval of the published version of the manuscript and all agree to be accountable for all aspects of the manuscript.

Corresponding author

Correspondence to Emily Steinhagen.

Ethics declarations

Disclosures

Drs. William Kethman, Katherine Bingmer, Asya Ofshteyn, Ronald Charles, and Emily Steinhagen have no conflicts of interest or financial ties, relevant to the material in this manuscript, to disclose. Dr. Sharon Stein has received a Physician’s Foundation grant for work unrelated to the topic of this manuscript and support from Stryker Corporation for travel expenses. Dr. David Dietz has received compensation as faculty for an educational course with Johnson & Johnson – Medical Device Business Services, Inc..

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kethman, W.C., Bingmer, K.E., Ofshteyn, A. et al. Effects of surgical approach on short- and long-term outcomes in early-stage rectal cancer: a multicenter, propensity score-weighted cohort study. Surg Endosc 36, 5833–5839 (2022). https://doi.org/10.1007/s00464-022-09033-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-022-09033-z

Keywords

Search

Navigation