Surgical Endoscopy

, Volume 30, Issue 10, pp 4405–4415 | Cite as

Predictors for regional lymph node metastasis in T1 rectal cancer: a population-based SEER analysis

  • Walter Brunner
  • Bernhard Widmann
  • Lukas Marti
  • Ignazio Tarantino
  • Bruno M. Schmied
  • Rene Warschkow



Local resection of early-stage rectal cancer significantly reduces perioperative morbidity compared with radical resection. Identifying patients at risk of regional lymph node metastasis (LNM) is crucial for long-term survival after local resection.


Patients after oncological resection of T1 rectal cancer were identified in the Surveillance, Epidemiology, and End Results register 2004–2012. Potential predictors of LNM and its impact on cancer-specific survival were assessed in logistic and Cox regression with and without multivariable adjustment.


In total, 1593 patients with radical resection of T1 rectal cancer and a minimum of 12 retrieved regional lymph nodes were identified. The overall LNM rate was 16.3 % (N = 260). A low risk of LNM was observed for small tumor size (P = 0.002), low tumor grade (P = 0.002) and higher age (P = 0.012) in multivariable analysis. The odds ratio for a tumor size exceeding 1.5 cm was 1.49 [95 % confidence interval (CI) 1.06–2.13], for G2 and G3/G4 carcinomas 1.69 (95 % CI 1.07–2.82) and 2.72 (95 % CI 1.50–5.03), and for 65- to 79-year-old and over 80-year-old patients 0.65 (95 % CI 0.43–0.96) and 0.39 (95 % CI 0.18–0.77), respectively. Five-year cancer-specific survival for patients with LNM was 90.0 % (95 % CI 85.3–95.0 %) and for patients without LNM 97.1 % (95 % CI 95.9–98.2 %, hazard ratio = 3.21, 95 % CI 1.82–5.69, P < 0.001).


In this population-based analysis, favorable cancer-specific survival rates were observed in nodal-negative and nodal-positive T1 rectal cancer patients after primary radical resection. The predictive value of tumor size, grading and age for LNM should be considered in medical decision making about local resection.


Rectal cancer Lymph node metastasis Surveillance, Epidemiology, and End Results (SEER) 



The authors thank the National Cancer Institute for providing the Surveillance, Epidemiology, and End Results (SEER) data set.

Compliance with ethical standards


Drs. Walter Brunner, Bernhard Widmann, Lukas Marti, Ignazio Tarantino, Bruno M. Schmied and Rene Warschkow have no conflicts of interest or financial ties to disclose.


  1. 1.
    Siegel R, Naishadham D, Jemal A (2012) Cancer statistics, 2012. CA Cancer J Clin 62:10–29CrossRefPubMedGoogle Scholar
  2. 2.
    Andersson J, Abis G, Gellerstedt M, Angenete E, Angeras U, Cuesta MA, Jess P, Rosenberg J, Bonjer HJ, Haglind E (2014) Patient-reported genitourinary dysfunction after laparoscopic and open rectal cancer surgery in a randomized trial (COLOR II). Br J Surg 101:1272–1279CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Emmertsen KJ, Laurberg S (2012) Low anterior resection syndrome score: development and validation of a symptom-based scoring system for bowel dysfunction after low anterior resection for rectal cancer. Ann Surg 255:922–928CrossRefPubMedGoogle Scholar
  4. 4.
    Greenblatt DY, Rajamanickam V, Pugely AJ, Heise CP, Foley EF, Kennedy GD (2011) Short-term outcomes after laparoscopic-assisted proctectomy for rectal cancer: results from the ACS NSQIP. J Am Coll Surg 212:844–854CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Pachler J, Wille-Jorgensen P (2012) Quality of life after rectal resection for cancer, with or without permanent colostomy. Cochrane Database Syst Rev 12:cd004323PubMedGoogle Scholar
  6. 6.
    van der Pas MH, Haglind E, Cuesta MA, Furst A, Lacy AM, Hop WC, Bonjer HJ, Group COcLoORIS (2013) Laparoscopic versus open surgery for rectal cancer (COLOR II): short-term outcomes of a randomised, phase 3 trial. Lancet Oncol 14:210–218CrossRefPubMedGoogle Scholar
  7. 7.
    Monson JR, Weiser MR, Buie WD, Chang GJ, Rafferty JF, Buie WD, Rafferty J (2013) Practice parameters for the management of rectal cancer (revised). Dis Colon Rectum 56:535–550CrossRefPubMedGoogle Scholar
  8. 8.
    Garcia-Aguilar J, Pollack J, Lee SH, Hernandez de Anda E, Mellgren A, Wong WD, Finne CO, Rothenberger DA, Madoff RD (2002) Accuracy of endorectal ultrasonography in preoperative staging of rectal tumors. Dis Colon Rectum 45:10–15CrossRefPubMedGoogle Scholar
  9. 9.
    Bosch SL, Teerenstra S, de Wilt JH, Cunningham C, Nagtegaal ID (2013) Predicting lymph node metastasis in pT1 colorectal cancer: a systematic review of risk factors providing rationale for therapy decisions. Endoscopy 45:827–834CrossRefPubMedGoogle Scholar
  10. 10.
    Bach SP, Hill J, Monson JR, Simson JN, Lane L, Merrie A, Warren B, Mortensen NJ, Association of Coloproctology of Great Britain Ireland Transanal Endoscopic Microsurgery Collaboration (2009) A predictive model for local recurrence after transanal endoscopic microsurgery for rectal cancer. Br J Surg 96:280–290CrossRefPubMedGoogle Scholar
  11. 11.
    Greenberg JA, Shibata D, Herndon JE 2nd, Steele GD Jr, Mayer R, Bleday R (2008) Local excision of distal rectal cancer: an update of cancer and leukemia group B 8984. Dis Colon Rectum 51:1185–1191CrossRefPubMedGoogle Scholar
  12. 12.
    Nash GM, Weiser MR, Guillem JG, Temple LK, Shia J, Gonen M, Wong WD, Paty PB (2009) Long-term survival after transanal excision of T1 rectal cancer. Dis Colon Rectum 52:577–582CrossRefPubMedGoogle Scholar
  13. 13.
    You YN, Baxter NN, Stewart A, Nelson H (2007) Is the increasing rate of local excision for stage I rectal cancer in the United States justified?: a nationwide cohort study from the National Cancer Database. Ann Surg 245:726–733CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Flanigan RC, Salmon SE, Blumenstein BA, Bearman SI, Roy V, McGrath PC, Caton JR Jr, Munshi N, Crawford ED (2001) Nephrectomy followed by interferon alfa-2b compared with interferon alfa-2b alone for metastatic renal-cell cancer. N Engl J Med 345:1655–1659CrossRefPubMedGoogle Scholar
  15. 15.
    Wingo PA, Jamison PM, Hiatt RA, Weir HK, Gargiullo PM, Hutton M, Lee NC, Hall HI (2003) Building the infrastructure for nationwide cancer surveillance and control–a comparison between the National Program of Cancer Registries (NPCR) and the Surveillance, Epidemiology, and End Results (SEER) Program (United States). Cancer Causes Control 14:175–193CrossRefPubMedGoogle Scholar
  16. 16.
    Fritz A, Percy C, Jack A, Shanmugaratnam K, Sobin L, Parkin DM, Whelan S (2000) International classification of disease for oncology. World Health Organization, GenevaGoogle Scholar
  17. 17.
    Tarantino I, Warschkow R, Worni M, Merati-Kashani K, Koberle D, Schmied BM, Muller SA, Steffen T, Cerny T, Guller U (2012) Elevated preoperative CEA is associated with worse survival in stage I-III rectal cancer patients. Br J Cancer 107:266–274CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Cleveland WS, Devlin SJ (1988) Locally-weighted regression: an approach to regression analysis by local fitting. J Am Stat Assoc 83:596–610CrossRefGoogle Scholar
  19. 19.
    Grambsch PM, Therneau TM (1994) Proportional hazards tests and diagnostics based on weighted residuals. Biometrika 81:515–526CrossRefGoogle Scholar
  20. 20.
    Hahnloser D, Wolff BG, Larson DW, Ping J, Nivatvongs S (2005) Immediate radical resection after local excision of rectal cancer: an oncologic compromise? Dis Colon Rectum 48:429–437CrossRefPubMedGoogle Scholar
  21. 21.
    Mellgren A, Sirivongs P, Rothenberger DA, Madoff RD, Garcia-Aguilar J (2000) Is local excision adequate therapy for early rectal cancer? Dis Colon Rectum 43:1064–1071CrossRefPubMedGoogle Scholar
  22. 22.
    Willett CG, Compton CC, Shellito PC, Efird JT (1994) Selection factors for local excision or abdominoperineal resection of early stage rectal cancer. Cancer 73:2716–2720CrossRefPubMedGoogle Scholar
  23. 23.
    Hase K, Shatney C, Johnson D, Trollope M, Vierra M (1993) Prognostic value of tumor “budding” in patients with colorectal cancer. Dis Colon Rectum 36:627–635CrossRefPubMedGoogle Scholar
  24. 24.
    Kudo S (1993) Endoscopic mucosal resection of flat and depressed types of early colorectal cancer. Endoscopy 25:455–461CrossRefPubMedGoogle Scholar
  25. 25.
    Aschele C, Cionini L, Lonardi S, Pinto C, Cordio S, Rosati G, Artale S, Tagliagambe A, Ambrosini G, Rosetti P, Bonetti A, Negru ME, Tronconi MC, Luppi G, Silvano G, Corsi DC, Bochicchio AM, Chiaulon G, Gallo M, Boni L (2011) Primary tumor response to preoperative chemoradiation with or without oxaliplatin in locally advanced rectal cancer: pathologic results of the STAR-01 randomized phase III trial. J Clin Oncol 29:2773–2780CrossRefPubMedGoogle Scholar
  26. 26.
    Gerard JP, Azria D, Gourgou-Bourgade S, Martel-Laffay I, Hennequin C, Etienne PL, Vendrely V, Francois E, de La Roche G, Bouche O, Mirabel X, Denis B, Mineur L, Berdah JF, Mahe MA, Becouarn Y, Dupuis O, Lledo G, Montoto-Grillot C, Conroy T (2010) Comparison of two neoadjuvant chemoradiotherapy regimens for locally advanced rectal cancer: results of the phase III trial ACCORD 12/0405-Prodige 2. J Clin Oncol 28:1638–1644CrossRefPubMedGoogle Scholar
  27. 27.
    Marusch F, Koch A, Schmidt U, Zippel R, Kuhn R, Wolff S, Pross M, Wierth A, Gastinger I, Lippert H (2002) Routine use of transrectal ultrasound in rectal carcinoma: results of a prospective multicenter study. Endoscopy 34:385–390CrossRefPubMedGoogle Scholar
  28. 28.
    Akasu T, Iinuma G, Takawa M, Yamamoto S, Muramatsu Y, Moriyama N (2009) Accuracy of high-resolution magnetic resonance imaging in preoperative staging of rectal cancer. Ann Surg Oncol 16:2787–2794CrossRefPubMedGoogle Scholar
  29. 29.
    Kim NK, Kim MJ, Park JK, Park SI, Min JS (2000) Preoperative staging of rectal cancer with MRI: accuracy and clinical usefulness. Ann Surg Oncol 7:732–737CrossRefPubMedGoogle Scholar
  30. 30.
    Bipat S, Glas AS, Slors FJ, Zwinderman AH, Bossuyt PM, Stoker J (2004) Rectal cancer: local staging and assessment of lymph node involvement with endoluminal US, CT, and MR imaging—a meta-analysis. Radiology 232:773–783CrossRefPubMedGoogle Scholar
  31. 31.
    Nascimbeni R, Burgart LJ, Nivatvongs S, Larson DR (2002) Risk of lymph node metastasis in T1 carcinoma of the colon and rectum. Dis Colon Rectum 45:200–206CrossRefPubMedGoogle Scholar
  32. 32.
    Nivatvongs S (2000) Surgical management of early colorectal cancer. World J Surg 24:1052–1055CrossRefPubMedGoogle Scholar
  33. 33.
    Son HJ, Song SY, Lee WY, Yang SS, Park SH, Yang MH, Yoon SH, Chun HK (2008) Characteristics of early colorectal carcinoma with lymph node metastatic disease. Hepatogastroenterology 55:1293–1297PubMedGoogle Scholar
  34. 34.
    Albert MR, Atallah SB, deBeche-Adams TC, Izfar S, Larach SW (2013) Transanal minimally invasive surgery (TAMIS) for local excision of benign neoplasms and early-stage rectal cancer: efficacy and outcomes in the first 50 patients. Dis Colon Rectum 56:301–307CrossRefPubMedGoogle Scholar
  35. 35.
    Tsai BM, Finne CO, Nordenstam JF, Christoforidis D, Madoff RD, Mellgren A (2010) Transanal endoscopic microsurgery resection of rectal tumors: outcomes and recommendations. Dis Colon Rectum 53:16–23CrossRefPubMedGoogle Scholar
  36. 36.
    Tarantino I, Hetzer FH, Warschkow R, Zund M, Stein HJ, Zerz A (2008) Local excision and endoscopic posterior mesorectal resection versus low anterior resection in T1 rectal cancer. Br J Surg 95:375–380CrossRefPubMedGoogle Scholar
  37. 37.
    van der Zaag ES, Bouma WH, Tanis PJ, Ubbink DT, Bemelman WA, Buskens CJ (2012) Systematic review of sentinel lymph node mapping procedure in colorectal cancer. Ann Surg Oncol 19:3449–3459CrossRefPubMedGoogle Scholar
  38. 38.
    Zerz A, Muller-Stich BP, Beck J, Linke GR, Tarantino I, Lange J (2006) Endoscopic posterior mesorectal resection after transanal local excision of T1 carcinomas of the lower third of the rectum. Dis Colon Rectum 49:919–924CrossRefPubMedGoogle Scholar
  39. 39.
    Stitzenberg KB, Sanoff HK, Penn DC, Meyers MO, Tepper JE (2013) Practice patterns and long-term survival for early-stage rectal cancer. J Clin Oncol 31:4276–4282CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Walter Brunner
    • 1
  • Bernhard Widmann
    • 1
  • Lukas Marti
    • 1
  • Ignazio Tarantino
    • 1
    • 2
  • Bruno M. Schmied
    • 1
  • Rene Warschkow
    • 1
    • 3
  1. 1.Department of General, Visceral, Endocrine and Transplantation SurgeryKantonsspital St. GallenSt. GallenSwitzerland
  2. 2.Department of General, Abdominal and Transplant SurgeryUniversity of HeidelbergHeidelbergGermany
  3. 3.Institute of Medical Biometry and InformaticsUniversity of HeidelbergHeidelbergGermany

Personalised recommendations