Annals of Surgical Oncology

, Volume 20, Issue 6, pp 1806–1815 | Cite as

Long-term Results of Rectal Cancer Surgery with a Systematical Operative Approach

  • Marilyne M. Lange
  • Joseph E. Martz
  • Beverly Ramdeen
  • Vicki Brooks
  • Kwadwo Boachie-Adjei
  • Cornelis J. H. van de Velde
  • Warren E. Enker
Colorectal Cancer



Variabilities of both oncologic and functional outcomes are major problems after rectal cancer treatment. Standardized techniques might produce more consistent surgical quality. This study reports outcomes during a 20-year period resulting from a systematically applied surgical approach.


Between 1990 and 2010, 368 rectal cancer patients, treated with total mesorectal excision conducted in a standardized, stepwise approach, were prospectively entered into a database. Influence of time period, surgeon, tumor and anastomotic height, and resection type was evaluated with multivariable regression analyses adjusting for age, disease stage, diversion, and (neo)adjuvant treatment. Function outcome questionnaires were sent to 50 patients at least 5 years after surgery.


Five-year overall survival was 76.4 %. Local and distant recurrence rates were 5.2 % and 22.1 %. Anastomotic leakage occurred in 5.4 % of patients treated with low anterior resection (n = 259). Time period, surgeon, tumor and anastomotic height, diversion, and abdominoperineal resection were not independent risk factors for any of these outcome measures. Both preoperative and postoperative radiotherapy were independently associated with increased risk of metastases (P = 0.035, hazard ratio (HR) = 3.04; and P = 0.029, HR = 3.59). Function questionnaires were completed by 38 of 50 patients (76 %). One of 13 nonirradiated patients reported mild fecal incontinence compared with 20 of 25 irradiated patients reporting mostly moderate-severe incontinence (P < 0.001).


Systematically applied surgical dissection results consistently in excellent oncologic outcomes with enhanced function outcomes. The findings suggest that in the presence of highly disciplined surgery, radiotherapy might make a smaller contribution to oncologic outcome, while leading to serious adverse effects.


Rectal Cancer Fecal Incontinence Total Mesorectal Excision Rectal Cancer Patient Circumferential Resection Margin 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work has been approved by the Institutional Review Board of Beth Israel Medical Center and was supported by the Dorothy and Lawrence Kryger Surgical Oncology Research Fund.

Conflicts of interest



  1. 1.
    Heald RJ. A new approach to rectal cancer. Br J Hosp Med. 1979;22(3):277–81.PubMedGoogle Scholar
  2. 2.
    Hermanek P, Hermanek PJ. Role of the surgeon as a variable in the treatment of rectal cancer. Semin Surg Oncol. 2000;19(4):329–35.PubMedCrossRefGoogle Scholar
  3. 3.
    Martling A, Cedermark B, Johansson H, Rutqvist LE, Holm T. The surgeon as a prognostic factor after the introduction of total mesorectal excision in the treatment of rectal cancer. Br J Surg. 2002;89(8):1008–13.PubMedCrossRefGoogle Scholar
  4. 4.
    Mack LA, Temple WJ. Education is the key to quality of surgery for rectal cancer. Eur J Surg Oncol. 2005;31(6):636–44.PubMedCrossRefGoogle Scholar
  5. 5.
    Sant M, Allemani C, Santaquilani M, Knijn A, Marchesi F, Capocaccia R. EUROCARE-4. Survival of cancer patients diagnosed in 1995–1999. Results and commentary. Eur J Cancer. 2009;45(6):931–91.PubMedCrossRefGoogle Scholar
  6. 6.
    Giacomantonio CA, Temple WJ. Quality of cancer surgery: challenges and controversies. Surg Oncol Clin N Am. 2000;9(1):51–60, vii.PubMedGoogle Scholar
  7. 7.
    Hermanek P, Wiebelt H, Staimmer D, Riedl S. Prognostic factors of rectum carcinoma–experience of the german multicentre study SGCRC. German Study Group Colo-Rectal Carcinoma. Tumori. 1995;81(3 Suppl):60–4.PubMedGoogle Scholar
  8. 8.
    Leonard D, Penninckx F, Fieuws S, Jouret-Mourin A, Sempoux C, Jehaes C, Van Eycken E. Factors predicting the quality of total mesorectal excision for rectal cancer. Ann Surg. 2010;252(6):982–8.PubMedCrossRefGoogle Scholar
  9. 9.
    Nagtegaal ID, van de Velde CJ, Marijnen CA, van Krieken JH, Quirke P. Low rectal cancer: a call for a change of approach in abdominoperineal resection. J Clin Oncol. 2005;23(36):9257–64.PubMedCrossRefGoogle Scholar
  10. 10.
    Marr R, Birbeck K, Garvican J, Macklin CP, Tiffin NJ, Parsons WJ, Dixon MF, Mapstone NP, Sebag-Montefiore D, Scott N, Johnston D, Sagar P, Finan P, Quirke P. The modern abdominoperineal excision: the next challenge after total mesorectal excision. Ann Surg. 2005;242(1):74–82.PubMedCrossRefGoogle Scholar
  11. 11.
    Pahlman L, Bohe M, Cedermark B, Dahlberg M, Lindmark G, Sjodahl R, Ojerskog B, Damber L, Johansson R. The Swedish Rectal Cancer Registry. Br J Surg. 2007;94(10):1285–92.PubMedCrossRefGoogle Scholar
  12. 12.
    Alberts JC, Parvaiz A, Moran BJ. Predicting risk and diminishing the consequences of anastomotic dehiscence following rectal resection. Colorectal Dis. 2003;5(5):478–82.PubMedCrossRefGoogle Scholar
  13. 13.
    Paun BC, Cassie S, MacLean AR, Dixon E, Buie WD. Postoperative complications following surgery for rectal cancer. Ann Surg. 2010;251(5):807–18.PubMedCrossRefGoogle Scholar
  14. 14.
    Peeters KC, van de Velde CJ, Leer JW, Martijn H, Junggeburt JM, Kranenbarg EK, Steup WH, Wiggers T, Rutten HJ, Marijnen CA. Late side effects of short-course preoperative radiotherapy combined with total mesorectal excision for rectal cancer: increased bowel dysfunction in irradiated patients–a Dutch Colorectal Cancer Group study. J Clin Oncol. 2005;23(25):6199–206.PubMedCrossRefGoogle Scholar
  15. 15.
    Lange MM, den Dulk M, Bossema ER, Maas CP, Peeters KC, Rutten HJ, Klein KE, Marijnen CA, van de Velde CJ. Risk factors for faecal incontinence after rectal cancer treatment. Br J Surg. 2007;94(10):1278–84.PubMedCrossRefGoogle Scholar
  16. 16.
    Bretagnol F, Troubat H, Laurent C, Zerbib F, Saric J, Rullier E. Long-term functional results after sphincter-saving resection for rectal cancer. Gastroenterol Clin Biol. 2004;28(2):155–9.PubMedCrossRefGoogle Scholar
  17. 17.
    Wallner C, Lange MM, Bonsing BA, Maas CP, Wallace CN, Dabhoiwala NF, Rutten HJ, Lamers WH, DeRuiter MC, van de Velde CJ. The role of damage to the levator ani nerve during rectal cancer surgery in the development of fecal and urinary incontinence. J Clin Oncol. 2008;26:4466–72.PubMedCrossRefGoogle Scholar
  18. 18.
    Lindsetmo RO, Delaney CP. A standardized technique for laparoscopic rectal resection. J Gastrointest Surg. 2009;13(11):2059–63.PubMedCrossRefGoogle Scholar
  19. 19.
    Enker WE. Potency, cure, and local control in the operative treatment of rectal cancer. Arch Surg. 1992;127(12):1396–401.PubMedCrossRefGoogle Scholar
  20. 20.
    Enker WE, Thaler HT, Cranor ML, Polyak T. Total mesorectal excision in the operative treatment of carcinoma of the rectum. J Am Coll Surg. 1995;181(4):335–46.PubMedGoogle Scholar
  21. 21.
    Enker WE. Total mesorectal excision–the new golden standard of surgery for rectal cancer. Ann Med. 1997;29(2):127–33.PubMedGoogle Scholar
  22. 22.
    Engstrom PF, Arnoletti JP, Benson AB III, Chen YJ, Choti MA, Cooper HS, Covey A, Dilawari RA, Early DS, Enzinger PC, Fakih MG, Fleshman J Jr, Fuchs C, Grem JL, Kiel K, Knol JA, Leong LA, Lin E, Mulcahy MF, Rao S, Ryan DP, Saltz L, Shibata D, Skibber JM, Sofocleous C, Thomas J, Venook AP, Willett C. NCCN Clinical Practice Guidelines in Oncology: Rectal cancer. J Natl Compr Canc Netw. 2009;7(8):838–81.PubMedGoogle Scholar
  23. 23.
    Sato K, Sato T. The vascular and neuronal composition of the lateral ligament of the rectum and the rectosacral fascia. Surg Radiol Anat. 1991;13(1):17–22.PubMedCrossRefGoogle Scholar
  24. 24.
    Hida J, Yasutomi M, Maruyama T, Fujimoto K, Uchida T, Okuno K. Lymph node metastases detected in the mesorectum distal to carcinoma of the rectum by the clearing method: justification of total mesorectal excision. J Am Coll Surg. 1997;184(6):584–8.PubMedGoogle Scholar
  25. 25.
    Enker WE. Cancer of the rectum: primary and adjuvant therapy. Fazio VW (ed) Current therapy in colon and rectal cancer. Philadelphia: Decker, B.C., 1990;120–30.Google Scholar
  26. 26.
    Adam IJ, Mohamdee MO, Martin IG, Scott N, Finan PJ, Johnston D, Dixon MF, Quirke P. Role of circumferential margin involvement in the local recurrence of rectal cancer. Lancet. 1994;344(8924):707–11.PubMedCrossRefGoogle Scholar
  27. 27.
    National workgroup for gastrointestinal tumours. Dutch National Guideline for Rectal Cancer (Version 2.0). www oncoline nl 2008.Google Scholar
  28. 28.
    Adjuvant radiotherapy for rectal cancer: a systematic overview of 8,507 patients from 22 randomised trials. Lancet. 2001;358(9290):1291–304.Google Scholar
  29. 29.
    Figueredo A, Zuraw L, Wong RK, Agboola O, Rumble RB, Tandan V. The use of preoperative radiotherapy in the management of patients with clinically resectable rectal cancer: a practice guideline. BMC Med. 2003;1:1.PubMedCrossRefGoogle Scholar
  30. 30.
    Roh MS, Colangelo LH, O’Connell MJ, Yothers G, Deutsch M, Allegra CJ, Kahlenberg MS, Baez-Diaz L, Ursiny CS, Petrelli NJ, Wolmark N. Preoperative multimodality therapy improves disease-free survival in patients with carcinoma of the rectum: NSABP R-03. J Clin Oncol. 2009;27(31):5124–30.PubMedCrossRefGoogle Scholar
  31. 31.
    Sauer R, Becker H, Hohenberger W, Rodel C, Wittekind C, Fietkau R, Martus P, Tschmelitsch J, Hager E, Hess CF, Karstens JH, Liersch T, Schmidberger H, Raab R. Preoperative versus postoperative chemoradiotherapy for rectal cancer. N Engl J Med. 2004;351(17):1731–40.PubMedCrossRefGoogle Scholar
  32. 32.
    Mathis KL, Larson DW, Dozois EJ, Cima RR, Huebner M, Haddock MG, Nelson H, Pemberton JH. Outcomes following surgery without radiotherapy for rectal cancer. Br J Surg. 2012;99:137–143.PubMedCrossRefGoogle Scholar
  33. 33.
    Taylor FG, Quirke P, Heald RJ, Moran B, Blomqvist L, Swift I, Sebag-Montefiore DJ, Tekkis P, Brown G. Preoperative high-resolution magnetic resonance imaging can identify good prognosis stage I, II, and III rectal cancer best managed by surgery alone: a prospective, multicenter, European study. Ann Surg 2011;253(4):711–9.PubMedCrossRefGoogle Scholar
  34. 34.
    Fisher B, Wolmark N, Rockette H, Redmond C, Deutsch M, Wickerham DL, Fisher ER, Caplan R, Jones J, Lerner H. Postoperative adjuvant chemotherapy or radiation therapy for rectal cancer: results from NSABP Protocol R-01. J Natl Cancer Inst. 1988;80(1):21–9.PubMedCrossRefGoogle Scholar
  35. 35.
    Inoue Y, Ojima E, Watanabe H, Hiro J, Toiyama Y, Kobayashi M, Miki C, Kusunoki M. Does preoperative chemo-radiotherapy enhance the expression of vascular endothelial growth factor in patients with rectal cancer? Oncol Rep. 2007;18(2):369–75.PubMedGoogle Scholar
  36. 36.
    Park JS, Qiao L, Su ZZ, Hinman D, Willoughby K, McKinstry R, Yacoub A, Duigou GJ, Young CS, Grant S, Hagan MP, Ellis E, Fisher PB, Dent P. Ionizing radiation modulates vascular endothelial growth factor (VEGF) expression through multiple mitogen activated protein kinase dependent pathways. Oncogene. 2001;20(25):3266–80.PubMedCrossRefGoogle Scholar
  37. 37.
    Nozue M, Isaka N, Fukao K. Over-expression of vascular endothelial growth factor after preoperative radiation therapy for rectal cancer. Oncol Rep. 2001;8(6):1247–9.PubMedGoogle Scholar
  38. 38.
    Pollack J, Holm T, Cedermark B, Altman D, Holmstrom B, Glimelius B, Mellgren A. Late adverse effects of short-course preoperative radiotherapy in rectal cancer. Br J Surg. 2006;93(12):1519–25.PubMedCrossRefGoogle Scholar
  39. 39.
    Marijnen CA, Kapiteijn E, van de Velde CJ, Martijn H, Steup WH, Wiggers T, Kranenbarg EK, Leer JW. Acute side effects and complications after short-term preoperative radiotherapy combined with total mesorectal excision in primary rectal cancer: report of a multicenter randomized trial. J Clin Oncol. 2002;20(3):817–25.PubMedCrossRefGoogle Scholar
  40. 40.
    Vuong T, Devic S, Podgorsak E. High-dose rate endorectal brachytherapy as a neoadjuvant treatment for patients with resectable rectal cancer. Clin Oncol (R Coll Radiol). 2007;19(9):701–5.CrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2013

Authors and Affiliations

  • Marilyne M. Lange
    • 1
    • 2
  • Joseph E. Martz
    • 3
  • Beverly Ramdeen
    • 3
  • Vicki Brooks
    • 3
  • Kwadwo Boachie-Adjei
    • 3
  • Cornelis J. H. van de Velde
    • 4
  • Warren E. Enker
    • 3
  1. 1.Department of Surgery and The Cancer CenterBeth Israel Medical CenterNew YorkUSA
  2. 2.Department of SurgeryZaans Medisch CentrumZaandamThe Netherlands
  3. 3.Colorectal Service, Department of Surgery and the Cancer CenterBeth Israel Medical Center, Albert Einstein College of MedicineNew YorkUSA
  4. 4.Department of SurgeryLeiden University Medical CenterLeidenThe Netherlands

Personalised recommendations