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Published in: Surgical Endoscopy 6/2013

01-06-2013

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

Authors: Marco Ettore Allaix, Alberto Arezzo, Paola Cassoni, Massimiliano Mistrangelo, Giuseppe Giraudo, Mario Morino

Published in: Surgical Endoscopy | Issue 6/2013

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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.
Literature
1.
go back to reference MacFarlane JK, Ryall RDH, Heald RJ (1993) Mesorectal excision for rectal cancer. Lancet 341:457–460CrossRefPubMed MacFarlane JK, Ryall RDH, Heald RJ (1993) Mesorectal excision for rectal cancer. Lancet 341:457–460CrossRefPubMed
2.
go back to reference Heald RJ, Moran BJ, Ryall RDH, Sexton R, MacFarlane JK (1998) The Basingstoke experience of total mesorectal excision, 1978–1997. Arch Surg 133:894–899CrossRefPubMed Heald RJ, Moran BJ, Ryall RDH, Sexton R, MacFarlane JK (1998) The Basingstoke experience of total mesorectal excision, 1978–1997. Arch Surg 133:894–899CrossRefPubMed
3.
go back to reference 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 26:415–421CrossRefPubMed 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 26:415–421CrossRefPubMed
4.
go back to reference 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 237:335–342PubMed 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 237:335–342PubMed
5.
go back to reference Schwenk W, Haase O, Neudecker J, Müller JM (2005) Short term benefits for laparoscopic colorectal resection. Cochrane Database Syst Rev (3):CD003145 Schwenk W, Haase O, Neudecker J, Müller JM (2005) Short term benefits for laparoscopic colorectal resection. Cochrane Database Syst Rev (3):CD003145
6.
go back to reference 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 142:298–303CrossRefPubMed 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 142:298–303CrossRefPubMed
7.
go back to reference 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 34:498–504CrossRefPubMed 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 34:498–504CrossRefPubMed
9.
go back to reference Poon JTC, Law WL (2009) Laparoscopic resection for rectal cancer: a review. Ann Surg Oncol 16:3038–3047CrossRefPubMed Poon JTC, Law WL (2009) Laparoscopic resection for rectal cancer: a review. Ann Surg Oncol 16:3038–3047CrossRefPubMed
10.
go back to reference 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–S116CrossRefPubMed 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–S116CrossRefPubMed
11.
go back to reference 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 35:497–503CrossRefPubMed 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 35:497–503CrossRefPubMed
12.
go back to reference 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 249:82–86CrossRefPubMed 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 249:82–86CrossRefPubMed
13.
go back to reference 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 19:1460–1467CrossRefPubMed 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 19:1460–1467CrossRefPubMed
14.
go back to reference 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 19:892–896CrossRefPubMed 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 19:892–896CrossRefPubMed
15.
go back to reference 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 51:385–391CrossRefPubMed 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 51:385–391CrossRefPubMed
16.
go back to reference 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 58:133–140CrossRefPubMed 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 58:133–140CrossRefPubMed
17.
go back to reference 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 25:3061–3068CrossRefPubMed 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 25:3061–3068CrossRefPubMed
18.
go back to reference 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 50:464–471CrossRefPubMed 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 50:464–471CrossRefPubMed
19.
go back to reference 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 15:2418–2425CrossRefPubMed 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 15:2418–2425CrossRefPubMed
20.
go back to reference 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 96:982–989CrossRefPubMed 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 96:982–989CrossRefPubMed
21.
go back to reference 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 52:558–566CrossRefPubMed 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 52:558–566CrossRefPubMed
22.
go back to reference 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 27:3109–3116CrossRefPubMed 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 27:3109–3116CrossRefPubMed
23.
go back to reference 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 99:433–441CrossRefPubMed 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 99:433–441CrossRefPubMed
24.
go back to reference NICE Improving Outcomes in Colorectal Cancer, Manual Update, London: National Institute for Clinical Excellence, May 2004 NICE Improving Outcomes in Colorectal Cancer, Manual Update, London: National Institute for Clinical Excellence, May 2004
25.
go back to reference 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 93:583–596CrossRefPubMed 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 93:583–596CrossRefPubMed
26.
go back to reference 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 106:209–216PubMed 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 106:209–216PubMed
27.
go back to reference 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 37:373–376CrossRefPubMed 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 37:373–376CrossRefPubMed
28.
go back to reference Wong JH, Severino R, Honnebier MB, Tom P, Namiki TS (1999) Number of nodes examined and staging accuracy in colorectal carcinoma. J Clin Oncol 17:2896–2900PubMed Wong JH, Severino R, Honnebier MB, Tom P, Namiki TS (1999) Number of nodes examined and staging accuracy in colorectal carcinoma. J Clin Oncol 17:2896–2900PubMed
29.
go back to reference 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 10:157–164PubMed 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 10:157–164PubMed
30.
go back to reference 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 4:29CrossRefPubMed 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 4:29CrossRefPubMed
31.
go back to reference 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 137:206–210CrossRefPubMed 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 137:206–210CrossRefPubMed
32.
go back to reference 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 61:426–431CrossRefPubMed 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 61:426–431CrossRefPubMed
33.
go back to reference 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 20:1729–1734CrossRefPubMed 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 20:1729–1734CrossRefPubMed
34.
go back to reference 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 32:45–50CrossRefPubMed 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 32:45–50CrossRefPubMed
35.
go back to reference 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 10:213–218CrossRefPubMed 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 10:213–218CrossRefPubMed
36.
go back to reference Jakub JW, Russell G, Tillman CL, Lariscy C (2009) Colon cancer and low lymph node count. Who is to blame? Arch Surg 144:1115–1120CrossRefPubMed Jakub JW, Russell G, Tillman CL, Lariscy C (2009) Colon cancer and low lymph node count. Who is to blame? Arch Surg 144:1115–1120CrossRefPubMed
37.
go back to reference 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 97:219–225CrossRefPubMed 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 97:219–225CrossRefPubMed
38.
go back to reference 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 23:53–59CrossRefPubMed 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 23:53–59CrossRefPubMed
39.
go back to reference 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 19:157–163PubMed 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 19:157–163PubMed
40.
go back to reference 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 245:543–552CrossRefPubMed 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 245:543–552CrossRefPubMed
41.
go back to reference 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 247:365–371CrossRefPubMed 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 247:365–371CrossRefPubMed
42.
go back to reference 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 17:2847–2855CrossRefPubMed 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 17:2847–2855CrossRefPubMed
43.
go back to reference 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 19:3895–3902PubMed 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 19:3895–3902PubMed
44.
go back to reference 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 46:975–981CrossRefPubMed 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 46:975–981CrossRefPubMed
45.
go back to reference 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 15:3118–3123CrossRefPubMed 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 15:3118–3123CrossRefPubMed
46.
go back to reference 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 248:968–978CrossRefPubMed 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 248:968–978CrossRefPubMed
47.
go back to reference 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 248:1067–1073CrossRefPubMed 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 248:1067–1073CrossRefPubMed
48.
go back to reference 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 74:796–802CrossRefPubMed 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 74:796–802CrossRefPubMed
49.
go back to reference 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 100:1530–1533CrossRefPubMed 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 100:1530–1533CrossRefPubMed
50.
go back to reference 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 13:113–121CrossRefPubMed 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 13:113–121CrossRefPubMed
51.
go back to reference 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 255:70–78CrossRefPubMed 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 255:70–78CrossRefPubMed
Metadata
Title
Metastatic lymph node ratio as a prognostic factor after laparoscopic total mesorectal excision for extraperitoneal rectal cancer
Authors
Marco Ettore Allaix
Alberto Arezzo
Paola Cassoni
Massimiliano Mistrangelo
Giuseppe Giraudo
Mario Morino
Publication date
01-06-2013
Publisher
Springer-Verlag
Published in
Surgical Endoscopy / Issue 6/2013
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-012-2694-5

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