Evaluation of the prognostic relevance of the recommended minimum number of lymph nodes in colorectal cancer-a propensity score analysis.
Colorectal cancer
Disease-free survival
Lymph nodes
Overall survival
Propensity score analysis
Journal
International journal of colorectal disease
ISSN: 1432-1262
Titre abrégé: Int J Colorectal Dis
Pays: Germany
ID NLM: 8607899
Informations de publication
Date de publication:
Apr 2021
Apr 2021
Historique:
accepted:
05
01
2021
pubmed:
18
1
2021
medline:
24
6
2021
entrez:
17
1
2021
Statut:
ppublish
Résumé
Nodal status in colorectal cancer (CRC) is an important prognostic factor, and adequate lymph node (LN) staging is crucial. Whether the number of resected and analysed LN has a direct impact on overall survival (OS), cancer-specific survival (CSS) and disease-free survival (DFS) is much discussed. Guidelines request a minimum number of 12 LN to be analysed. Whether that threshold marks a prognostic relevant cut-off remains unknown. Patients operated for stage I-III CRC were identified from a prospectively maintained database. The impact of the number of analysed LN on OS, CSS and DFS was assessed using Cox regression and propensity score analysis. Of the 687 patients, 81.8% had ≥ 12 LN resected and analysed. Median LN yield was 17.0 (IQR 13.0-23.0). Resection and analysis of ≥ 12 LN was associated with improved OS (HR = 0.73, 95% CI: 0.56-0.95, p = 0.033), CSS (HR 0.52, 95% CI: 0.31-0.85, p = 0.030) and DFS (HR = 0.73, 95% CI: 0.57-0.95, p = 0.030) in multivariate Cox analysis. After adjusting for biasing factors with propensity score matching, resection of ≥ 12 LN was significantly associated with improved OS (HR = 0.59; 95% CI: 0.43-0.81; p = 0.002), CSS (HR = 0.34; 95% CI: 0.20-0.60; p < 0.001) and DFS (HR = 0.55; 95% CI: 0.41-0.74; p < 0.001) compared to patients with < 12 LN. Eliminating biasing factors by a propensity score matching analysis underlines the prognostic importance of the number of analysed LN. The set threshold marks the minimum number of required LN but nevertheless represents a cut-off regarding outcome in stage I-III CRC. This analysis therefore highlights the significance and importance of adherence to surgical oncological standards.
Identifiants
pubmed: 33454816
doi: 10.1007/s00384-021-03835-8
pii: 10.1007/s00384-021-03835-8
pmc: PMC7952332
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
779-789Références
Fischer J, Hellmich G, Jackisch T, Puffer E, Zimmer J, Bleyl D, Kittner T, Witzigmann H, Stelzner S (2015) Outcome for stage II and III rectal and colon cancer equally good after treatment improvement over three decades. Int J Color Dis 30(6):797–806
Siegel RL, Miller KD, Jemal A (2017) Colorectal cancer mortality rates in adults aged 20 to 54 years in the United States, 1970–2014. JAMA 318(6):572–574
pubmed: 28787497
pmcid: 5817468
UICC, I.U.A.C., International Union Against Cancer (2009) TNM classification of malignant tumours, 7th edn. Wiley-Blackwell, West-Sussex
Brierley JD, Gospodarowicz M., Wittekind C, eds. International Union Against Cancer (UICC). TNM Classification of Malignant Tumours, 8th edn. Oxford: Wiley Blackwell, 2017
Labianca R et al (2013) Early colon cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 24(Suppl 6):vi64–vi72
pubmed: 24078664
Vogel JD, Eskicioglu C, Weiser MR, Feingold DL, Steele SR (2017) The American Society of Colon and Rectal Surgeons Clinical Practice Guidelines for the Treatment of Colon Cancer. Dis Colon Rectum 60(10):999–1017
pubmed: 28891842
Amin MB, Greene FL, Edge SB, Compton CC, Gershenwald JE, Brookland RK, Meyer L, Gress DM, Byrd DR, Winchester DP (2017) The eighth edition AJCC cancer staging manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin 67(2):93–99
pubmed: 28094848
pmcid: 28094848
Fielding LP, Arsenault PA, Chapuis PH, Dent O, Gathright B, Hardcastle JD, Hermanek P, Jass JR, Newland RC (1991) Clinicopathological staging for colorectal cancer: an International Documentation System (IDS) and an International Comprehensive Anatomical Terminology (ICAT). J Gastroenterol Hepatol 6(4):325–344
pubmed: 1912440
Swanson RS, Compton CC, Stewart AK, Bland KI (2003) The prognosis of T3N0 colon cancer is dependent on the number of lymph nodes examined. Ann Surg Oncol 10(1):65–71
pubmed: 12513963
Sarli L, Bader G, Iusco D, Salvemini C, Mauro DD, Mazzeo A, Regina G, Roncoroni L (2005) Number of lymph nodes examined and prognosis of TNM stage II colorectal cancer. Eur J Cancer 41(2):272–279
pubmed: 15661553
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(6):433–441
pubmed: 17374833
Moore J, Hyman N, Callas P, Littenberg B (2010) Staging error does not explain the relationship between the number of lymph nodes in a colon cancer specimen and survival. Surgery 147(3):358–365
pubmed: 19962166
Lykke J, Jess P, Roikjaer O (2015) Increased lymph node yield is associated with improved survival in rectal cancer irrespective of neoadjuvant treatment: results from a National Cohort Study. Dis Colon Rectum 58(9):823–830
pubmed: 26252843
Sobin LH, Gospodarowicz M., Wittekind C, eds. International Union Against Cancer (UICC), TNM Classification of Malignant Tumours, 7th edn. New York: Wiley, 2009
Joffe MM, Rosenbaum PR (1999) Invited commentary: propensity scores. Am J Epidemiol 150(4):327–333
pubmed: 10453808
Rosenbaum PR (1987) Model-Based Direct Adjustment. J Am Stat Assoc 82(398):387–394
Rosenbaum PR (1989) Optimal matching for observational studies. J Am Stat Assoc 84(408):1024–1032
Hansen BB, Klopfer SO (2006) Optimal full matching and related designs via network flows. J Comput Graph Stat 15(3):609–627
Sekhon JS (2011) Multivariate and propensity score matching software with automated balance optimization: the matching package for R. J Stat Softw 42(7):1–52
Burnham KP, Anderson DR (eds) (2002) Model selection and multimodel inference: a practical information-theoretic approach, Second edn. Springer, New York
Anderson DR (2008) Model based inference in the life sciences: a primer on evidence. Springer, New York
Chambless LE, Diao G (2006) Estimation of time-dependent area under the ROC curve for long-term risk prediction. Stat Med 25(20):3474–3486
pubmed: 16220486
Chen SL, Bilchik AJ (2006) More extensive nodal dissection improves survival for stages I to III of colon cancer: a population-based study. Ann Surg 244(4):602–610
pubmed: 16998369
pmcid: 1856560
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(3):219–225
pubmed: 15687365
Maurer CA, Dietrich D, Schilling MK, Metzger U, Laffer U, Buchmann P, Lerf B, Villiger P, Melcher G, Klaiber C, Bilat C, Brauchli P, Terracciano L, Kessler K (2017) Prospective multicenter registration study of colorectal cancer: significant variations in radicality and oncosurgical quality-Swiss Group for Clinical Cancer Research Protocol SAKK 40/00. Int J Colorectal Dis 32(1):57–74
pubmed: 27714521
VoyerTE Le, Sigurdson ER, Hanlon AL, Mayer RJ, Macdonald JS, Catalano PJ, Haller DG (2003) Colon cancer survival is associated with increasing number of lymph nodes analyzed: a secondary survey of intergroup trial INT-0089. J Clin Oncol 21(15):2912–2919
Babcock BD, Aljehani MA, Jabo B, Choi AH, Morgan JW, Selleck MJ, Luca F, Raskin E, Reeves ME, Garberoglio CA, Lum SS, Senthil M (2018) High-risk stage II colon cancer: not all risks are created equal. Ann Surg Oncol 25(7):1980–1985
pubmed: 29675762
Tsai HL, Huang CW, Chen CW, Yeh YS, Ma CJ, Wang JY (2016) Survival in resected stage II colorectal cancer is dependent on tumor depth, vascular invasion, postoperative CEA level, and the number of examined lymph nodes. World J Surg 40(4):1002–1009
pubmed: 26560149
Bockelman C, Engelmann BE, Kaprio T, Hansen TF, Glimelius B (2015) Risk of recurrence in patients with colon cancer stage II and III: a systematic review and meta-analysis of recent literature. Acta Oncol 54(1):5–16
pubmed: 25430983
Weixler B, Warschkow R, Güller U, Zettl A, von Holzen U, Schmied BM, Zuber M (2016) Isolated tumor cells in stage I & II colon cancer patients are associated with significantly worse disease-free and overall survival. BMC Cancer 16:16–106. https://doi.org/10.1186/s12885-016-2130-7
doi: 10.1186/s12885-016-2130-7
Pagès F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R, Mlecnik B, Kirilovsky A, Nilsson M, Damotte D, Meatchi T, Bruneval P, Cugnenc PH, Trajanoski Z, Fridman WH, Galon J (2005) Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 353(25):2654–2666
pubmed: 16371631
Gorog D, Nagy P, Peter A, Perner F (2003) Influence of obesity on lymph node recovery from rectal resection specimens. Pathol Oncol Res 9(3):180–183
pubmed: 14530812
Ostadi MA, Harnish JL, Stegienko S, Urbach DR (2007) Factors affecting the number of lymph nodes retrieved in colorectal cancer specimens. Surg Endosc 21(12):2142–2146
pubmed: 17522917
Wong SL (2009) Lymph node counts and survival rates after resection for colon and rectal cancer. Gastrointest Cancer Res 3(2 Suppl):S33–S35
pubmed: 19461921
pmcid: 2684729
Cahill RA, Lindsey I, Cunningham C (2010) Sentinel node mapping by colonic tattooing. Surg Endosc 24(9):2365–2366
pubmed: 20177923
Kang J, Park HS, Kim IK, Song Y, Baik SH, Sohn SK, Lee KY (2015) Effect of preoperative colonoscopic tattooing on lymph node harvest in T1 colorectal cancer. Int J Color Dis 30(10):1349–1355
Brown HG, Luckasevic TM, Medich DS, Celebrezze JP, Jones SM (2004) Efficacy of manual dissection of lymph nodes in colon cancer resections. Mod Pathol 17(4):402–406
pubmed: 14976530
Guller U, Zettl A, Worni M, Langer I, Cabalzar-Wondberg D, Viehl CT, Demartines N, Zuber M (2012) Molecular investigation of lymph nodes in colon cancer patients using one-step nucleic acid amplification (OSNA): a new road to better staging? Cancer 118(24):6039–6045
Wild JB, Iqbal N, Francombe J, Papettas T, Sanders DS, Ramcharan S (2017) Is it time for one-step nucleic acid amplification (OSNA) in colorectal cancer? A systematic review and meta-analysis. Tech Coloproctol 21(9):693–699
pubmed: 28887714
Croner RS, Geppert CI, Bader FG, Nitsche U, Späth C, Rosenberg R, Zettl A, Matias-Guiu X, Tarragona J, Güller U, Stürzl M, Zuber M (2014) Molecular staging of lymph node-negative colon carcinomas by one-step nucleic acid amplification (OSNA) results in upstaging of a quarter of patients in a prospective, European, multicentre study. Br J Cancer 110(10):2544–2550
pubmed: 24722182
pmcid: 4021519
Viehl CT, Guller U, Cecini R, Langer I, Ochsner A, Terracciano L, Riehle HM, Laffer U, Oertli D, Zuber M (2012) Sentinel lymph node procedure leads to upstaging of patients with resectable colon cancer: results of the Swiss prospective, multicenter study sentinel lymph node procedure in colon cancer. Ann Surg Oncol 19(6):1959–1965
pubmed: 22322951
Weixler B, Rickenbacher A, Raptis DA, Viehl CT, Guller U, Rueff J, Zettl A, Zuber M (2017) Sentinel lymph node mapping with isosulfan blue or indocyanine green in colon cancer shows comparable results and identifies patients with decreased survival: a prospective single-center trial. World J Surg 41(9):2378–2386
pubmed: 28508233
Hohenberger W, Weber K, Matzel K, Papadopoulos T, Merkel S (2009) Standardized surgery for colonic cancer: complete mesocolic excision and central ligation–technical notes and outcome. Colorectal Dis 11(4):354–364
pubmed: 19016817
West NP, Hohenberger W, Weber K, Perrakis A, Finan PJ, Quirke P (2010) Complete mesocolic excision with central vascular ligation produces an oncologically superior specimen compared with standard surgery for carcinoma of the colon. J Clin Oncol 28(2):272–278
pubmed: 19949013
Pelz JOW, Wagner J, Lichthardt S, Baur J, Kastner C, Matthes N, Germer CT, Wiegering A (2018) Laparoscopic right-sided colon resection for colon cancer-has the control group so far been chosen correctly? World J Surg Oncol 16(1):117
pubmed: 29954404
pmcid: 6022499
Bertelsen CA, Neuenschwander AU, Jansen JE, Wilhelmsen M, Kirkegaard-Klitbo A, Tenma JR, Bols B, Ingeholm P, Rasmussen LA, Jepsen LV, Iversen ER, Kristensen B, Gögenur I, Danish Colorectal Cancer Group (2015) Disease-free survival after complete mesocolic excision compared with conventional colon cancer surgery: a retrospective, population-based study. Lancet Oncol 16(2):161–168
pubmed: 25555421
Bertelsen CA, Neuenschwander AU, Jansen JE, Kirkegaard-Klitbo A, Tenma JR, Wilhelmsen M, Rasmussen LA, Jepsen LV, Kristensen B, Gögenur I, the Copenhagen Complete Mesocolic Excision Study (COMES), the Danish Colorectal Cancer Group (DCCG) (2016) Short-term outcomes after complete mesocolic excision compared with ‘conventional’ colonic cancer surgery. Br J Surg 103(5):581–589
pubmed: 26780563
Pox C, Aretz S, Bischoff SC, Graeven U, Hass M, Heußner P, Hohenberger W, Holstege A, Hübner J, Kolligs F, Kreis M, Lux P, Ockenga J, Porschen R, Post S, Rahner N, Reinacher-Schick A, Riemann JF, Sauer R, Sieg A, Scheppach W, Schmitt W, Schmoll HJ, Schulmann K, Tannapfel A, Schmiegel W; Leitlinienprogramm Onkologie der AWMF; Deutschen Krebsgesellschaft e. V; Deutschen Krebshilfe e. V.: S3-Leitlinie kolorektales Karzinom Version 1.0 – Juni 2013 AWMF Registernummer: 021/007OL. Z Gastroenterol 2013;51:753–854
Viehl CT, Ochsner A, von Holzen U, Cecini R, Langer I, Guller U, Laffer U, Oertli D, Zuber M (2010) Inadequate quality of surveillance after curative surgery for colon cancer. Ann Surg Oncol 17(10):2663–2669
Rueff J, Weixler B, Viehl CT, Ochsner A, Warschkow R, Gueller U, Mingrone W, Zuber M (2020) Improved quality of colon cancer surveillance after implementation of a personalized surveillance schedule. J Surg Oncol 122:529–537
pubmed: 32410263