Skip to main content

Advertisement

Log in

Metastatic lymph node ratio as a prognostic factor after laparoscopic total mesorectal excision for extraperitoneal rectal cancer

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

The lymph node ratio (LNR; number of positive nodes divided by total nodes harvested) has been demonstrated to be a prognostic factor in colon cancer, but its role in extraperitoneal rectal cancer is still debated; furthermore, no data are available on laparoscopic rectal resection. The aim of this study was to evaluate the prognostic impact of LNR on long-term outcomes after laparoscopic total mesorectal excision (LTME) for extraperitoneal cancer in consecutive patients with a 5-year minimum follow-up.

Methods

This study is a prospective analysis of consecutive patients who underwent LTME for adenocarcinoma of the extraperitoneal rectum.

Results

LTME was performed in 158 patients. The median number of LN harvested was 12 (range = 3–25). The proportion of specimens with fewer than 12 examined LN was significantly higher in patients who had neoadjuvant chemoradiotherapy (p < 0.001). During a median follow-up period of 122 months, the local recurrence rate was 8 %. At univariate analysis, disease-free survival and overall survival significantly decreased with increasing LNR (p < 0.001). Multivariate analysis showed that the distal margin ≤1 cm was the only independent predictor of local recurrence (p = 0.028). LNR (cutoff value = 0.25) and lymphovascular invasion were significant prognostic factors for both disease-free (p = 0.015 and p = 0.046, respectively) and overall survival (p = 0.031 and p = 0.040, respectively). Even in the subgroup of patients in whom fewer than 12 LN were examined, LNR confirmed its prognostic role, with a statistical trend toward worse disease-free survival and overall survival.

Conclusion

Metastatic LNR is an independent prognostic factor for disease-free survival and overall survival after LTME for extraperitoneal rectal cancer.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. MacFarlane JK, Ryall RDH, Heald RJ (1993) Mesorectal excision for rectal cancer. Lancet 341:457–460

    Article  CAS  PubMed  Google Scholar 

  2. Heald RJ, Moran BJ, Ryall RDH, Sexton R, MacFarlane JK (1998) The Basingstoke experience of total mesorectal excision, 1978–1997. Arch Surg 133:894–899

    Article  CAS  PubMed  Google Scholar 

  3. Huang MJ, Liang JL, Wang H, Kang L, Deng YH, Wang JP (2011) Laparoscopic-assisted versus open surgery for rectal cancer: a meta-analysis of randomized controlled trials on oncologic adequacy of resection and long-term oncologic outcomes. Int J Colorectal Dis 26:415–421

    Article  PubMed  Google Scholar 

  4. Morino M, Parini U, Giraudo G, Salval M, Brachet Contul R, Garrone C (2003) Laparoscopic total mesorectal excision: a consecutive series of 100 patients. Ann Surg 237:335–342

    PubMed  Google Scholar 

  5. Schwenk W, Haase O, Neudecker J, Müller JM (2005) Short term benefits for laparoscopic colorectal resection. Cochrane Database Syst Rev (3):CD003145

  6. Bonjer HJ, Hop WC, Nelson H, Sargent DJ, Lacy AM, Castells A, Guillou PJ, Thorpe H, Brown J, Delgado S, Kuhrij E, Haglind E, Påhlman L, Transatlantic Laparoscopically Assisted vs Open Colectomy Trials Study Group (2007) Laparoscopically assisted vs open colectomy for colon cancer: a meta-analysis. Arch Surg 142:298–303

    Article  PubMed  Google Scholar 

  7. Kuhry E, Schwenk W, Gaupset R, Romild U, Bonjer J (2008) Long-term outcome of laparoscopic surgery for colorectal cancer: a cochrane systematic review of randomised controlled trials. Cancer Treat Rev 34:498–504

    Article  PubMed  Google Scholar 

  8. Breukink S, Pierie JP, Wiggers T (2006) Laparoscopic versus open total mesorectal excision for rectal cancer. Cochrane Database Syst Rev CD005200. doi:10.1002/14651858.CD005200.pub2

  9. Poon JTC, Law WL (2009) Laparoscopic resection for rectal cancer: a review. Ann Surg Oncol 16:3038–3047

    Article  PubMed  Google Scholar 

  10. Staudacher C, Di PS, Tamburini A, Vignali A, Orsenigo E (2007) Total mesorectal excision (TME) with laparoscopic approach: 226 consecutive cases. Surg Oncol 16:S113–S116

    Article  PubMed  Google Scholar 

  11. Pugliese R, Di Lernia S, Sansonna F, Maggioni D, Ferrari GC, Magistro C, Costanzi A, De Carli S, Artale S, Pugliese F (2009) Laparoscopic resection for rectal adenocarcinoma. Eur J Surg Oncol 35:497–503

    Article  CAS  PubMed  Google Scholar 

  12. Ng KH, Ng DC, Cheung HY, Wong JC, Yau KK, Chung CC, Li MK (2009) Laparoscopic resection for rectal cancers: lessons learned from 579 cases. Ann Surg 249:82–86

    Article  PubMed  Google Scholar 

  13. Morino M, Allaix ME, Giraudo G, Corno F, Garrone C (2005) Laparoscopic versus open surgery for extraperitoneal rectal cancer: a prospective comparative study. Surg Endosc 19:1460–1467

    Article  CAS  PubMed  Google Scholar 

  14. Bretagnol F, Lelong B, Laurent C, Moutardier V, Rullier A, Monges G, Delpero JR, Rullier E (2005) The oncological safety of laparoscopic total mesorectal excision with sphincter preservation for rectal carcinoma. Surg Endosc 19:892–896

    Article  CAS  PubMed  Google Scholar 

  15. Strohlein MA, Grutzner KU, Jauch KW, Heiss MM (2008) Comparison of laparoscopic vs open access surgery in patients with rectal cancer: a prospective analysis. Dis Colon Rectum 51:385–391

    Article  PubMed  Google Scholar 

  16. Araujo SE, da Silva eSousa AH Jr, de Campos FG, Habr-Gama A, Dumarco RB, Caravatto PP, Nahas SC, da Silva J, Kiss DR, Gama-Rodrigues JJ (2003) Conventional approach x laparoscopic abdominoperineal resection for rectal cancer treatment after neoadjuvant chemoradiation: results of a prospective randomized trial. Rev Hosp Clin Fac Med Sao Paulo 58:133–140

    Article  PubMed  Google Scholar 

  17. Jayne DG, Guillou PJ, Thorpe H, Quirke P, Copeland J, Smith AM, Heath RM, Brown JM, UK MRC CLASICC Trial Group (2007) Randomized trial of laparoscopic-assisted resection of colorectal carcinoma: 3-year results of the UK MRC CLASICC Trial Group. J Clin Oncol 25:3061–3068

    Article  PubMed  Google Scholar 

  18. Braga M, Frasson M, Vignali A, Zuliani W, Capretti G, Di Carlo V (2007) Laparoscopic resection in rectal cancer patients: outcome and cost-benefit analysis. Dis Colon Rectum 50:464–471

    Article  PubMed  Google Scholar 

  19. Ng SS, Leung KL, Lee JF, Yiu RY, Li JC, Teoh AY (2008) Laparoscopic-assisted versus open abdominoperineal resection for low rectal cancer: a prospective randomized trial. Ann Surg Oncol 15:2418–2425

    Article  PubMed  Google Scholar 

  20. Lujan J, Valero G, Hernandez Q, Sanchez A, Frutos MD, Parrilla P (2009) Randomized clinical trial comparing laparoscopic and open surgery in patients with rectal cancer. Br J Surg 96:982–989

    Article  CAS  PubMed  Google Scholar 

  21. Ng SS, Leung KL, Lee JF, Yiu RY, Li JC, Hon SS (2009) 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 52:558–566

    Article  PubMed  Google Scholar 

  22. André T, Boni C, Navarro M, Tabernero J, Hickish T, Topham C, Bonetti A, Clingan P, Bridgewater J, Rivera F, de Gramont A (2009) Improved overall survival with oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment in stage II or III colon cancer in the MOSAIC trial. J Clin Oncol 27:3109–3116

    Article  PubMed  Google Scholar 

  23. Chang GJ, Rodriguez-Bigas MA, Skibber JM, Moyer VA (2007) Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst 99:433–441

    Article  PubMed  Google Scholar 

  24. NICE Improving Outcomes in Colorectal Cancer, Manual Update, London: National Institute for Clinical Excellence, May 2004

  25. Nelson H, Petrelli N, Carlin A, Couture J, Fleshman J, Guillem J, Miedema B, Ota D, Sargent D, National Cancer Institute Expert Panel (2001) Guidelines 2000 for colon and rectal cancer surgery. J Natl Cancer Inst 93:583–596

    Article  CAS  PubMed  Google Scholar 

  26. Goldstein NS, Sanford W, Coffey M, Layfield LJ (1996) Lymph node recovery from colorectal resection specimens removed for adenocarcinoma. Trends over time and a recommendation for a minimum number of lymph nodes to be recovered. Am J Clin Pathol 106:209–216

    CAS  PubMed  Google Scholar 

  27. Hernanz F, Revuelta S, Redondo C, Madrazo C, Castillo J, Gomez-Fleitas M (1994) Colorectal adenocarcinoma: quality of the assessment of lymph node metastases. Dis Colon Rectum 37:373–376

    Article  CAS  PubMed  Google Scholar 

  28. Wong JH, Severino R, Honnebier MB, Tom P, Namiki TS (1999) Number of nodes examined and staging accuracy in colorectal carcinoma. J Clin Oncol 17:2896–2900

    CAS  PubMed  Google Scholar 

  29. Evans MD, Barton K, Rees A, Stamatakis JD, Karandikar SS (2008) The impact of surgeon and pathologist on lymph node retrieval in colorectal cancer and its impact on survival for patients with Dukes’ stage B disease. Colorectal Dis 10:157–164

    CAS  PubMed  Google Scholar 

  30. Sermier A, Gervaz P, Egger JF, Dao M, Allal AS, Bonet M, Morel P (2006) Lymph node retrieval in abdominoperineal surgical specimen is radiation time-dependent. World J Surg Oncol 4:29

    Article  PubMed  Google Scholar 

  31. Wichmann MW, Muller C, Meyer G, Strauss T, Hornung HM, Lau-Werner U, Angele MK, Schildberg FW (2002) Effect of preoperative radiochemotherapy on lymph node retrieval after resection of rectal cancer. Arch Surg 137:206–210

    Article  PubMed  Google Scholar 

  32. Baxter NN, Morris AM, Rothenberger DA, Tepper JE (2005) Impact of preoperative radiation for rectal cancer on subsequent lymph node evaluation: a population-based analysis. Int J Radiat Oncol Biol Phys 61:426–431

    Article  PubMed  Google Scholar 

  33. Nagtegaal ID, van de Velde CJ, van der Worp E, Kapiteijn E, Quirke P, van Krieken JH (2002) Macroscopic evaluation of rectal cancer resection specimen: clinical significance of the pathologist in quality control. J Clin Oncol 20:1729–1734

    Article  PubMed  Google Scholar 

  34. Rullier A, Laurent C, Capdepont M, Vendrely V, Belleannée G, Bioulac-Sage P, Rullier E (2008) Lymph nodes after preoperative chemoradiotherapy for rectal carcinoma: number, status, and impact on survival. Am J Surg Pathol 32:45–50

    Article  PubMed  Google Scholar 

  35. Joseph NE, Sigurdson ER, Hanlon AL, Wang H, Mayer RJ, MacDonald JS, Catalano PJ, Haller DG (2003) Accuracy of determining nodal negativity in colorectal cancer on the basis of the number of nodes retrieved on resection. Ann Surg Oncol 10:213–218

    Article  PubMed  Google Scholar 

  36. Jakub JW, Russell G, Tillman CL, Lariscy C (2009) Colon cancer and low lymph node count. Who is to blame? Arch Surg 144:1115–1120

    Article  PubMed  Google Scholar 

  37. Baxter NN, Virnig DJ, Rothenberger DA, Morris AM, Jessurun J, Virnig BA (2005) Lymph node evaluation in colorectal cancer patients: a population-based study. J Natl Cancer Inst 97:219–225

    Article  PubMed  Google Scholar 

  38. Gelos M, Gelhaus J, Mehnert P, Bonhag G, Sand M, Philippou S, Mann B (2008) Factors influencing lymph node harvest in colorectal surgery. Int J Colorectal Dis 23:53–59

    Article  CAS  PubMed  Google Scholar 

  39. Tepper JE, O’Connell MJ, Niedzwiecki D, Hollis D, Compton C, Benson AB 3rd, 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 19:157–163

    CAS  PubMed  Google Scholar 

  40. Marchet A, Mocellin S, Ambrosi A, Morgagni P, Garcea D, Marrelli D, Roviello F, de Manzoni G, Minicozzi A, Natalini G, De Santis F, Baiocchi L, Coniglio A, Nitti D, Italian Research Group for Gastric Cancer (IRGGC) (2007) The ratio between metastatic and examined lymph nodes (N Ratio) is an independent prognostic factor in gastric cancer regardless of the type of lymphadenectomy: results of an Italian multicentric study in 1853 patients. Ann Surg 245:543–552

    Article  PubMed  Google Scholar 

  41. Mariette C, Piessen G, Briez N, Triboulet JP (2008) The number of metastatic lymph nodes and the ratio between metastatic and examined lymph nodes are independent prognostic factors in oesophageal cancer regardless of neoadjuvant chemoradiation or lympadenectomy extent. Ann Surg 247:365–371

    Article  PubMed  Google Scholar 

  42. Ceelen W, Van Nieuwenhove Y, Pattyn P (2010) Prognostic value of the lymph node ratio in stage III colorectal cancer: a systematic review. Ann Surg Oncol 17:2847–2855

    Article  CAS  PubMed  Google Scholar 

  43. Stocchi L, Nelson H, Sargent DJ, O’Connell MJ, Tepper JE, Krook JE, Beart R Jr, North Central Cancer Treatment Group (2001) Impact of surgical and pathologic variables in rectal cancer: a United States Community and Cooperative Group report. J Clin Oncol 19:3895–3902

    CAS  PubMed  Google Scholar 

  44. Edler D, Ohrling K, Hallström M, Karlberg M, Ragnhammar P (2007) The number of analyzed lymph nodes - a prognostic factor in colorectal cancer. Acta Oncol 46:975–981

    Article  PubMed  Google Scholar 

  45. Peng JJ, Xu Y, Guan ZQ, Zhu J, Wang M, Cai G, Sheng W, Cai S (2008) Prognostic significance of the metastatic lymph node ratio in node-positive rectal cancer. Ann Surg Oncol 15:3118–3123

    Article  PubMed  Google Scholar 

  46. Rosenberg R, Friederichs J, Schuster T, Gertler R, Maak M, Becker K, Grebner A, Ulm K, Höfler H, Nekarda H, Siewert JR (2008) Prognosis of patients with colorectal cancer is associated with lymph node ratio. A single-center analysis of 3026 patients over a 25-year time period. Ann Surg 248:968–978

    Article  PubMed  Google Scholar 

  47. Peschaud F, Benoist S, Julié C, Beauchet A, Penna C, Rougier P, Nordlinger B (2008) Prognosis of patients with colorectal cancer is associated with lymph node ratio: a single-center analysis of 3026 patients over a 25-year time period. Ann Surg 248:1067–1073

    Article  PubMed  Google Scholar 

  48. Kim YS, Kim JH, Yoon SM, Choi EK, Ahn SD, Lee SW, Kim JC, Yu CS, Kim HC, Kim TW, Chang HM (2009) Lymph node ratio as a prognostic factor in patients with stage III rectal cancer treated with total mesorectal excision followed by chemoradiotherapy. Int J Radiat Oncol Biol Phys 74:796–802

    Article  PubMed  Google Scholar 

  49. Moug SJ, Saldanha JD, McGregor JR, Balsitis M, Diament RH (2009) Positive lymph node retrieval ratio optimises patient staging in colorectal cancer. Br J Cancer 100:1530–1533

    Article  CAS  PubMed  Google Scholar 

  50. Priolli DG, Cardinalli IA, Pereira JA, Alfredo CH, Margarido NF, Martinez CA (2009) Metastatic lymph node ratio as an independent prognostic variable in colorectal cancer: study of 113 patients. Tech Coloproctol 13:113–121

    Article  CAS  PubMed  Google Scholar 

  51. Huh JW, Kim YJ, Kim HR (2012) Distribution of lymph mode metastases is an independent predictor of survival for sigmoid colon and rectal cancer. Ann Surg 255:70–78

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

No funds, grants or support was received to complete the study.

Disclosures

Marco Ettore Allaix, Alberto Arezzo, Paola Cassoni, Massimiliano Mistrangelo, Giuseppe Giraudo, and Mario Morino have no conflicts of interest or financial ties to disclose.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mario Morino.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Allaix, M.E., Arezzo, A., Cassoni, P. et al. Metastatic lymph node ratio as a prognostic factor after laparoscopic total mesorectal excision for extraperitoneal rectal cancer. Surg Endosc 27, 1957–1967 (2013). https://doi.org/10.1007/s00464-012-2694-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-012-2694-5

Keywords

Navigation