Skip to main content
Top
Published in: Journal of Experimental & Clinical Cancer Research 1/2017

Open Access 01-12-2017 | Research

Nomogram integrating gene expression signatures with clinicopathological features to predict survival in operable NSCLC: a pooled analysis of 2164 patients

Authors: Jian Wu, Lizhi Zhou, Lixia Huang, Jincui Gu, Shaoli Li, Baomo Liu, Jinlun Feng, Yanbin Zhou

Published in: Journal of Experimental & Clinical Cancer Research | Issue 1/2017

Login to get access

Abstract

Background

The current tumor-node-metastasis (TNM) staging system is insufficient to predict outcome of patients with operable Non-Small Cell Lung Cancer (NSCLC) owing to its phenotypic and genomic heterogeneity. Integrating genomic signatures with clinicopathological factors may provide more detailed evaluation of prognosis.

Methods

All 2164 clinically annotated NSCLC samples (1326 in the training set and 838 in the validation set) with corresponding microarray data from 17 cohorts were pooled to develop and validate a clinicopathologic-genomic nomogram based on Cox regression model. Two computational methods were applied to these samples to capture expression pattern of genomic signatures representing biological statuses. Model performance was measured by the concordance index (C-index) and calibration plot. Risk group stratification was proposed for the nomogram.

Results

Multivariable analysis of the training set identified independent factors including age, TNM stage, combined prognostic classifier, non-overlapping signature, and the ratio of neutrophil to plasma cells. The C-index of the nomogram for predicting survival was statistically superior to that of the TNM stage (training set, 0.686 vs 0.627, respectively; P < .001; validation set, 0.689 vs 0.638, respectively; P < .001). The calibration plots showed that the predicted 1-, 3- and 5-year survival probabilities agreed well with the actual observations. Stratifying patients into three risk groups detected significant differences among survival curves.

Conclusions

These findings offer preliminary evidence that genomic data provide independent and complementary prognostic information and incorporation of this information can refine prognosis in NSCLC. Prospective studies are required to further explore the value of this composite model for prognostic stratification and tailored therapeutic strategies.
Appendix
Available only for authorised users
Literature
1.
go back to reference Stewart B, Wild CP. World cancer report 2014. Lyon: International Agency for Research on Cancer, World Health Organization; 2014. Stewart B, Wild CP. World cancer report 2014. Lyon: International Agency for Research on Cancer, World Health Organization; 2014.
3.
go back to reference Pignon JP, Tribodet H, Scagliotti GV, Douillard JY, Shepherd FA, Stephens RJ, Dunant A, Torri V, Rosell R, Seymour L, et al. Lung adjuvant cisplatin evaluation: a pooled analysis by the LACE Collaborative Group. J Clin Oncol. 2008;26:3552–9.CrossRefPubMed Pignon JP, Tribodet H, Scagliotti GV, Douillard JY, Shepherd FA, Stephens RJ, Dunant A, Torri V, Rosell R, Seymour L, et al. Lung adjuvant cisplatin evaluation: a pooled analysis by the LACE Collaborative Group. J Clin Oncol. 2008;26:3552–9.CrossRefPubMed
4.
go back to reference Strauss GM, Herndon 2nd JE, Maddaus MA, Johnstone DW, Johnson EA, Harpole DH, Gillenwater HH, Watson DM, Sugarbaker DJ, Schilsky RL, et al. Adjuvant paclitaxel plus carboplatin compared with observation in stage IB non-small-cell lung cancer: CALGB 9633 with the Cancer and Leukemia Group B, Radiation Therapy Oncology Group, and North Central Cancer Treatment Group Study Groups. J Clin Oncol. 2008;26:5043–51.CrossRefPubMedPubMedCentral Strauss GM, Herndon 2nd JE, Maddaus MA, Johnstone DW, Johnson EA, Harpole DH, Gillenwater HH, Watson DM, Sugarbaker DJ, Schilsky RL, et al. Adjuvant paclitaxel plus carboplatin compared with observation in stage IB non-small-cell lung cancer: CALGB 9633 with the Cancer and Leukemia Group B, Radiation Therapy Oncology Group, and North Central Cancer Treatment Group Study Groups. J Clin Oncol. 2008;26:5043–51.CrossRefPubMedPubMedCentral
5.
go back to reference Butts CA, Ding K, Seymour L, Twumasi-Ankrah P, Graham B, Gandara D, Johnson DH, Kesler KA, Green M, Vincent M, et al. Randomized phase III trial of vinorelbine plus cisplatin compared with observation in completely resected stage IB and II non-small-cell lung cancer: updated survival analysis of JBR-10. J Clin Oncol. 2010;28:29–34.CrossRefPubMed Butts CA, Ding K, Seymour L, Twumasi-Ankrah P, Graham B, Gandara D, Johnson DH, Kesler KA, Green M, Vincent M, et al. Randomized phase III trial of vinorelbine plus cisplatin compared with observation in completely resected stage IB and II non-small-cell lung cancer: updated survival analysis of JBR-10. J Clin Oncol. 2010;28:29–34.CrossRefPubMed
6.
go back to reference Douillard J-Y, Rosell R, De Lena M, Carpagnano F, Ramlau R, Gonzáles-Larriba JL, Grodzki T, Pereira JR, Le Groumellec A, Lorusso V, et al. Adjuvant vinorelbine plus cisplatin versus observation in patients with completely resected stage IB–IIIA non-small-cell lung cancer (Adjuvant Navelbine International Trialist Association [ANITA]): a randomised controlled trial. Lancet Oncol. 2006;7:719–27.CrossRefPubMed Douillard J-Y, Rosell R, De Lena M, Carpagnano F, Ramlau R, Gonzáles-Larriba JL, Grodzki T, Pereira JR, Le Groumellec A, Lorusso V, et al. Adjuvant vinorelbine plus cisplatin versus observation in patients with completely resected stage IB–IIIA non-small-cell lung cancer (Adjuvant Navelbine International Trialist Association [ANITA]): a randomised controlled trial. Lancet Oncol. 2006;7:719–27.CrossRefPubMed
7.
go back to reference Consonni D, Pierobon M, Gail MH, Rubagotti M, Rotunno M, Goldstein A, Goldin L, Lubin J, Wacholder S, Caporaso NE, et al. Lung cancer prognosis before and after recurrence in a population-based setting. J Natl Cancer Inst. 2015;107:djv059.CrossRefPubMedPubMedCentral Consonni D, Pierobon M, Gail MH, Rubagotti M, Rotunno M, Goldstein A, Goldin L, Lubin J, Wacholder S, Caporaso NE, et al. Lung cancer prognosis before and after recurrence in a population-based setting. J Natl Cancer Inst. 2015;107:djv059.CrossRefPubMedPubMedCentral
8.
go back to reference Liang W, Zhang L, Jiang G, Wang Q, Liu L, Liu D, Wang Z, Zhu Z, Deng Q, Xiong X, et al. Development and validation of a nomogram for predicting survival in patients with resected non-small-cell lung cancer. J Clin Oncol. 2015;33:861–9.CrossRefPubMed Liang W, Zhang L, Jiang G, Wang Q, Liu L, Liu D, Wang Z, Zhu Z, Deng Q, Xiong X, et al. Development and validation of a nomogram for predicting survival in patients with resected non-small-cell lung cancer. J Clin Oncol. 2015;33:861–9.CrossRefPubMed
9.
go back to reference Birim O, Kappetein AP, Waleboer M, Puvimanasinghe JP, Eijkemans MJ, Steyerberg EW, Versteegh MI, Bogers AJ. Long-term survival after non-small cell lung cancer surgery: development and validation of a prognostic model with a preoperative and postoperative mode. J Thorac Cardiovasc Surg. 2006;132:491–8.CrossRefPubMed Birim O, Kappetein AP, Waleboer M, Puvimanasinghe JP, Eijkemans MJ, Steyerberg EW, Versteegh MI, Bogers AJ. Long-term survival after non-small cell lung cancer surgery: development and validation of a prognostic model with a preoperative and postoperative mode. J Thorac Cardiovasc Surg. 2006;132:491–8.CrossRefPubMed
10.
go back to reference Brambilla E, Le Teuff G, Marguet S, Lantuejoul S, Dunant A, Graziano S, Pirker R, Douillard JY, Le Chevalier T, Filipits M, et al. Prognostic Effect of Tumor Lymphocytic Infiltration in Resectable Non-Small-Cell Lung Cancer. J Clin Oncol. 2016;34:1223–30.CrossRefPubMed Brambilla E, Le Teuff G, Marguet S, Lantuejoul S, Dunant A, Graziano S, Pirker R, Douillard JY, Le Chevalier T, Filipits M, et al. Prognostic Effect of Tumor Lymphocytic Infiltration in Resectable Non-Small-Cell Lung Cancer. J Clin Oncol. 2016;34:1223–30.CrossRefPubMed
11.
12.
go back to reference Carter SL, Eklund AC, Kohane IS, Harris LN, Szallasi Z. A signature of chromosomal instability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nat Genet. 2006;38:1043–8.CrossRefPubMed Carter SL, Eklund AC, Kohane IS, Harris LN, Szallasi Z. A signature of chromosomal instability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nat Genet. 2006;38:1043–8.CrossRefPubMed
13.
go back to reference Chi JT, Wang Z, Nuyten DS, Rodriguez EH, Schaner ME, Salim A, Wang Y, Kristensen GB, Helland A, Borresen-Dale AL, et al. Gene expression programs in response to hypoxia: cell type specificity and prognostic significance in human cancers. PLoS Med. 2006;3:e47.CrossRefPubMedPubMedCentral Chi JT, Wang Z, Nuyten DS, Rodriguez EH, Schaner ME, Salim A, Wang Y, Kristensen GB, Helland A, Borresen-Dale AL, et al. Gene expression programs in response to hypoxia: cell type specificity and prognostic significance in human cancers. PLoS Med. 2006;3:e47.CrossRefPubMedPubMedCentral
14.
go back to reference Chang HY, Sneddon JB, Alizadeh AA, Sood R, West RB, Montgomery K, Chi JT, van de Rijn M, Botstein D, Brown PO. Gene expression signature of fibroblast serum response predicts human cancer progression: similarities between tumors and wounds. PLoS Biol. 2004;2:E7.CrossRefPubMedPubMedCentral Chang HY, Sneddon JB, Alizadeh AA, Sood R, West RB, Montgomery K, Chi JT, van de Rijn M, Botstein D, Brown PO. Gene expression signature of fibroblast serum response predicts human cancer progression: similarities between tumors and wounds. PLoS Biol. 2004;2:E7.CrossRefPubMedPubMedCentral
15.
go back to reference Ramaswamy S, Ross KN, Lander ES, Golub TR. A molecular signature of metastasis in primary solid tumors. Nat Genet. 2003;33:49–54.CrossRefPubMed Ramaswamy S, Ross KN, Lander ES, Golub TR. A molecular signature of metastasis in primary solid tumors. Nat Genet. 2003;33:49–54.CrossRefPubMed
16.
go back to reference Peng G, Chun-Jen Lin C, Mo W, Dai H, Park YY, Kim SM, Peng Y, Mo Q, Siwko S, Hu R, et al. Genome-wide transcriptome profiling of homologous recombination DNA repair. Nat Commun. 2014;5:3361.PubMedPubMedCentral Peng G, Chun-Jen Lin C, Mo W, Dai H, Park YY, Kim SM, Peng Y, Mo Q, Siwko S, Hu R, et al. Genome-wide transcriptome profiling of homologous recombination DNA repair. Nat Commun. 2014;5:3361.PubMedPubMedCentral
17.
go back to reference Chen JL, Lucas JE, Schroeder T, Mori S, Wu J, Nevins J, Dewhirst M, West M, Chi JT. The genomic analysis of lactic acidosis and acidosis response in human cancers. PLoS Genet. 2008;4:e1000293.CrossRefPubMedPubMedCentral Chen JL, Lucas JE, Schroeder T, Mori S, Wu J, Nevins J, Dewhirst M, West M, Chi JT. The genomic analysis of lactic acidosis and acidosis response in human cancers. PLoS Genet. 2008;4:e1000293.CrossRefPubMedPubMedCentral
18.
go back to reference Saal LH, Johansson P, Holm K, Gruvberger-Saal SK, She QB, Maurer M, Koujak S, Ferrando AA, Malmstrom P, Memeo L, et al. Poor prognosis in carcinoma is associated with a gene expression signature of aberrant PTEN tumor suppressor pathway activity. Proc Natl Acad Sci U S A. 2007;104:7564–9.CrossRefPubMedPubMedCentral Saal LH, Johansson P, Holm K, Gruvberger-Saal SK, She QB, Maurer M, Koujak S, Ferrando AA, Malmstrom P, Memeo L, et al. Poor prognosis in carcinoma is associated with a gene expression signature of aberrant PTEN tumor suppressor pathway activity. Proc Natl Acad Sci U S A. 2007;104:7564–9.CrossRefPubMedPubMedCentral
19.
go back to reference Coulouarn C, Factor VM, Thorgeirsson SS. Transforming growth factor-beta gene expression signature in mouse hepatocytes predicts clinical outcome in human cancer. Hepatology. 2008;47:2059–67.CrossRefPubMedPubMedCentral Coulouarn C, Factor VM, Thorgeirsson SS. Transforming growth factor-beta gene expression signature in mouse hepatocytes predicts clinical outcome in human cancer. Hepatology. 2008;47:2059–67.CrossRefPubMedPubMedCentral
20.
go back to reference Pittman J, Huang E, Dressman H, Horng CF, Cheng SH, Tsou MH, Chen CM, Bild A, Iversen ES, Huang AT, et al. Integrated modeling of clinical and gene expression information for personalized prediction of disease outcomes. Proc Natl Acad Sci U S A. 2004;101:8431–6.CrossRefPubMedPubMedCentral Pittman J, Huang E, Dressman H, Horng CF, Cheng SH, Tsou MH, Chen CM, Bild A, Iversen ES, Huang AT, et al. Integrated modeling of clinical and gene expression information for personalized prediction of disease outcomes. Proc Natl Acad Sci U S A. 2004;101:8431–6.CrossRefPubMedPubMedCentral
21.
go back to reference McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM, Statistics Subcommittee of the NCIEWGoCD. Reporting recommendations for tumor marker prognostic studies (REMARK). J Natl Cancer Inst. 2005;97:1180–4.CrossRefPubMed McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM, Statistics Subcommittee of the NCIEWGoCD. Reporting recommendations for tumor marker prognostic studies (REMARK). J Natl Cancer Inst. 2005;97:1180–4.CrossRefPubMed
22.
23.
go back to reference Fan C, Oh DS, Wessels L, Weigelt B, Nuyten DS, Nobel AB, van’t Veer LJ, Perou CM. Concordance among gene-expression-based predictors for breast cancer. N Engl J Med. 2006;355:560–9.CrossRefPubMed Fan C, Oh DS, Wessels L, Weigelt B, Nuyten DS, Nobel AB, van’t Veer LJ, Perou CM. Concordance among gene-expression-based predictors for breast cancer. N Engl J Med. 2006;355:560–9.CrossRefPubMed
24.
go back to reference Newman AM, Liu CL, Green MR, Gentles AJ, Feng W, Xu Y, Hoang CD, Diehn M, Alizadeh AA. Robust enumeration of cell subsets from tissue expression profiles. Nat Methods. 2015;12:453–7.CrossRefPubMedPubMedCentral Newman AM, Liu CL, Green MR, Gentles AJ, Feng W, Xu Y, Hoang CD, Diehn M, Alizadeh AA. Robust enumeration of cell subsets from tissue expression profiles. Nat Methods. 2015;12:453–7.CrossRefPubMedPubMedCentral
25.
go back to reference Schemper M, Smith TL. A note on quantifying follow-up in studies of failure time. Control Clin Trials. 1996;17:343–6.CrossRefPubMed Schemper M, Smith TL. A note on quantifying follow-up in studies of failure time. Control Clin Trials. 1996;17:343–6.CrossRefPubMed
26.
go back to reference Nevins JR, Potti A. Mining gene expression profiles: expression signatures as cancer phenotypes. Nat Rev Genet. 2007;8:601–9.CrossRefPubMed Nevins JR, Potti A. Mining gene expression profiles: expression signatures as cancer phenotypes. Nat Rev Genet. 2007;8:601–9.CrossRefPubMed
27.
go back to reference Rhodes DR, Chinnaiyan AM. Integrative analysis of the cancer transcriptome. Nat Genet. 2005;37(Suppl):S31–7.CrossRefPubMed Rhodes DR, Chinnaiyan AM. Integrative analysis of the cancer transcriptome. Nat Genet. 2005;37(Suppl):S31–7.CrossRefPubMed
28.
go back to reference Raponi M, Zhang Y, Yu J, Chen G, Lee G, Taylor JM, Macdonald J, Thomas D, Moskaluk C, Wang Y, Beer DG. Gene expression signatures for predicting prognosis of squamous cell and adenocarcinomas of the lung. Cancer Res. 2006;66:7466–72.CrossRefPubMed Raponi M, Zhang Y, Yu J, Chen G, Lee G, Taylor JM, Macdonald J, Thomas D, Moskaluk C, Wang Y, Beer DG. Gene expression signatures for predicting prognosis of squamous cell and adenocarcinomas of the lung. Cancer Res. 2006;66:7466–72.CrossRefPubMed
29.
go back to reference Sun Z, Wigle DA, Yang P. Non-overlapping and non-cell-type-specific gene expression signatures predict lung cancer survival. J Clin Oncol. 2008;26:877–83.CrossRefPubMed Sun Z, Wigle DA, Yang P. Non-overlapping and non-cell-type-specific gene expression signatures predict lung cancer survival. J Clin Oncol. 2008;26:877–83.CrossRefPubMed
30.
go back to reference Xie Y, Xiao G, Coombes KR, Behrens C, Solis LM, Raso G, Girard L, Erickson HS, Roth J, Heymach JV, et al. Robust gene expression signature from formalin-fixed paraffin-embedded samples predicts prognosis of non-small-cell lung cancer patients. Clin Cancer Res. 2011;17:5705–14.CrossRefPubMedPubMedCentral Xie Y, Xiao G, Coombes KR, Behrens C, Solis LM, Raso G, Girard L, Erickson HS, Roth J, Heymach JV, et al. Robust gene expression signature from formalin-fixed paraffin-embedded samples predicts prognosis of non-small-cell lung cancer patients. Clin Cancer Res. 2011;17:5705–14.CrossRefPubMedPubMedCentral
31.
go back to reference Lu Y, Lemon W, Liu PY, Yi Y, Morrison C, Yang P, Sun Z, Szoke J, Gerald WL, Watson M, et al. A Gene Expression Signature Predicts Survival of Patients with Stage I Non-Small Cell Lung Cancer. PLoS Med. 2006;3:e467.CrossRefPubMedPubMedCentral Lu Y, Lemon W, Liu PY, Yi Y, Morrison C, Yang P, Sun Z, Szoke J, Gerald WL, Watson M, et al. A Gene Expression Signature Predicts Survival of Patients with Stage I Non-Small Cell Lung Cancer. PLoS Med. 2006;3:e467.CrossRefPubMedPubMedCentral
32.
go back to reference Roepman P, Jassem J, Smit EF, Muley T, Niklinski J, van de Velde T, Witteveen AT, Rzyman W, Floore A, Burgers S, et al. An immune response enriched 72-gene prognostic profile for early-stage non-small-cell lung cancer. Clin Cancer Res. 2009;15:284–90.CrossRefPubMed Roepman P, Jassem J, Smit EF, Muley T, Niklinski J, van de Velde T, Witteveen AT, Rzyman W, Floore A, Burgers S, et al. An immune response enriched 72-gene prognostic profile for early-stage non-small-cell lung cancer. Clin Cancer Res. 2009;15:284–90.CrossRefPubMed
33.
go back to reference Mitra R, Lee J, Jo J, Milani M, McClintick JN, Edenberg HJ, Kesler KA, Rieger KM, Badve S, Cummings OW, et al. Prediction of postoperative recurrence-free survival in non-small cell lung cancer by using an internationally validated gene expression model. Clin Cancer Res. 2011;17:2934–46.CrossRefPubMedPubMedCentral Mitra R, Lee J, Jo J, Milani M, McClintick JN, Edenberg HJ, Kesler KA, Rieger KM, Badve S, Cummings OW, et al. Prediction of postoperative recurrence-free survival in non-small cell lung cancer by using an internationally validated gene expression model. Clin Cancer Res. 2011;17:2934–46.CrossRefPubMedPubMedCentral
34.
go back to reference Whitfield ML, Sherlock G, Saldanha AJ, Murray JI, Ball CA, Alexander KE, Matese JC, Perou CM, Hurt MM, Brown PO, Botstein D. Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol Biol Cell. 2002;13:1977–2000.CrossRefPubMedPubMedCentral Whitfield ML, Sherlock G, Saldanha AJ, Murray JI, Ball CA, Alexander KE, Matese JC, Perou CM, Hurt MM, Brown PO, Botstein D. Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol Biol Cell. 2002;13:1977–2000.CrossRefPubMedPubMedCentral
35.
go back to reference Chen DT, Hsu YL, Fulp WJ, Coppola D, Haura EB, Yeatman TJ, Cress WD. Prognostic and predictive value of a malignancy-risk gene signature in early-stage non-small cell lung cancer. J Natl Cancer Inst. 2011;103:1859–70.CrossRefPubMedPubMedCentral Chen DT, Hsu YL, Fulp WJ, Coppola D, Haura EB, Yeatman TJ, Cress WD. Prognostic and predictive value of a malignancy-risk gene signature in early-stage non-small cell lung cancer. J Natl Cancer Inst. 2011;103:1859–70.CrossRefPubMedPubMedCentral
36.
go back to reference Liu R, Wang X, Chen GY, Dalerba P, Gurney A, Hoey T, Sherlock G, Lewicki J, Shedden K, Clarke MF. The prognostic role of a gene signature from tumorigenic breast-cancer cells. N Engl J Med. 2007;356:217–26.CrossRefPubMed Liu R, Wang X, Chen GY, Dalerba P, Gurney A, Hoey T, Sherlock G, Lewicki J, Shedden K, Clarke MF. The prognostic role of a gene signature from tumorigenic breast-cancer cells. N Engl J Med. 2007;356:217–26.CrossRefPubMed
37.
go back to reference Li L, Wei Y, To C, Zhu CQ, Tong J, Pham NA, Taylor P, Ignatchenko V, Ignatchenko A, Zhang W, et al. Integrated omic analysis of lung cancer reveals metabolism proteome signatures with prognostic impact. Nat Commun. 2014;5:5469.CrossRefPubMed Li L, Wei Y, To C, Zhu CQ, Tong J, Pham NA, Taylor P, Ignatchenko V, Ignatchenko A, Zhang W, et al. Integrated omic analysis of lung cancer reveals metabolism proteome signatures with prognostic impact. Nat Commun. 2014;5:5469.CrossRefPubMed
38.
go back to reference Winter SC, Buffa FM, Silva P, Miller C, Valentine HR, Turley H, Shah KA, Cox GJ, Corbridge RJ, Homer JJ, et al. Relation of a hypoxia metagene derived from head and neck cancer to prognosis of multiple cancers. Cancer Res. 2007;67:3441–9.CrossRefPubMed Winter SC, Buffa FM, Silva P, Miller C, Valentine HR, Turley H, Shah KA, Cox GJ, Corbridge RJ, Homer JJ, et al. Relation of a hypoxia metagene derived from head and neck cancer to prognosis of multiple cancers. Cancer Res. 2007;67:3441–9.CrossRefPubMed
39.
go back to reference Navab R, Strumpf D, Bandarchi B, Zhu CQ, Pintilie M, Ramnarine VR, Ibrahimov E, Radulovich N, Leung L, Barczyk M, et al. Prognostic gene-expression signature of carcinoma-associated fibroblasts in non-small cell lung cancer. Proc Natl Acad Sci U S A. 2011;108:7160–5.CrossRefPubMedPubMedCentral Navab R, Strumpf D, Bandarchi B, Zhu CQ, Pintilie M, Ramnarine VR, Ibrahimov E, Radulovich N, Leung L, Barczyk M, et al. Prognostic gene-expression signature of carcinoma-associated fibroblasts in non-small cell lung cancer. Proc Natl Acad Sci U S A. 2011;108:7160–5.CrossRefPubMedPubMedCentral
40.
go back to reference Masiero M, Simoes FC, Han HD, Snell C, Peterkin T, Bridges E, Mangala LS, Wu SY, Pradeep S, Li D, et al. A core human primary tumor angiogenesis signature identifies the endothelial orphan receptor ELTD1 as a key regulator of angiogenesis. Cancer Cell. 2013;24:229–41.CrossRefPubMedPubMedCentral Masiero M, Simoes FC, Han HD, Snell C, Peterkin T, Bridges E, Mangala LS, Wu SY, Pradeep S, Li D, et al. A core human primary tumor angiogenesis signature identifies the endothelial orphan receptor ELTD1 as a key regulator of angiogenesis. Cancer Cell. 2013;24:229–41.CrossRefPubMedPubMedCentral
41.
go back to reference Hu J, Bianchi F, Ferguson M, Cesario A, Margaritora S, Granone P, Goldstraw P, Tetlow M, Ratcliffe C, Nicholson AG, et al. Gene expression signature for angiogenic and nonangiogenic non-small-cell lung cancer. Oncogene. 2005;24:1212–9.CrossRefPubMed Hu J, Bianchi F, Ferguson M, Cesario A, Margaritora S, Granone P, Goldstraw P, Tetlow M, Ratcliffe C, Nicholson AG, et al. Gene expression signature for angiogenic and nonangiogenic non-small-cell lung cancer. Oncogene. 2005;24:1212–9.CrossRefPubMed
42.
go back to reference Bild AH, Yao G, Chang JT, Wang Q, Potti A, Chasse D, Joshi MB, Harpole D, Lancaster JM, Berchuck A, et al. Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature. 2006;439:353–7.CrossRefPubMed Bild AH, Yao G, Chang JT, Wang Q, Potti A, Chasse D, Joshi MB, Harpole D, Lancaster JM, Berchuck A, et al. Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature. 2006;439:353–7.CrossRefPubMed
43.
go back to reference Gentles AJ, Newman AM, Liu CL, Bratman SV, Feng W, Kim D, Nair VS, Xu Y, Khuong A, Hoang CD, et al. The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat Med. 2015;21:938–45.CrossRefPubMedPubMedCentral Gentles AJ, Newman AM, Liu CL, Bratman SV, Feng W, Kim D, Nair VS, Xu Y, Khuong A, Hoang CD, et al. The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat Med. 2015;21:938–45.CrossRefPubMedPubMedCentral
44.
go back to reference Kratz JR, He J, Van Den Eeden SK, Zhu ZH, Gao W, Pham PT, Mulvihill MS, Ziaei F, Zhang H, Su B, et al. A practical molecular assay to predict survival in resected non-squamous, non-small-cell lung cancer: development and international validation studies. Lancet. 2012;379:823–32.CrossRefPubMedPubMedCentral Kratz JR, He J, Van Den Eeden SK, Zhu ZH, Gao W, Pham PT, Mulvihill MS, Ziaei F, Zhang H, Su B, et al. A practical molecular assay to predict survival in resected non-squamous, non-small-cell lung cancer: development and international validation studies. Lancet. 2012;379:823–32.CrossRefPubMedPubMedCentral
45.
go back to reference Goldstraw P, Chansky K, Crowley J, Rami-Porta R, Asamura H, Eberhardt WE, Nicholson AG, Groome P, Mitchell A, Bolejack V, et al. The IASLC Lung Cancer Staging Project: Proposals for Revision of the TNM Stage Groupings in the Forthcoming (Eighth) Edition of the TNM Classification for Lung Cancer. J Thorac Oncol. 2016;11:39–51.CrossRefPubMed Goldstraw P, Chansky K, Crowley J, Rami-Porta R, Asamura H, Eberhardt WE, Nicholson AG, Groome P, Mitchell A, Bolejack V, et al. The IASLC Lung Cancer Staging Project: Proposals for Revision of the TNM Stage Groupings in the Forthcoming (Eighth) Edition of the TNM Classification for Lung Cancer. J Thorac Oncol. 2016;11:39–51.CrossRefPubMed
46.
go back to reference Goldstraw P, Crowley J, Chansky K, Giroux DJ, Groome PA, Rami-Porta R, Postmus PE, Rusch V, Sobin L, International Association for the Study of Lung Cancer International Staging C, Participating I. The IASLC Lung Cancer Staging Project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM Classification of malignant tumours. J Thorac Oncol. 2007;2:706–14.CrossRefPubMed Goldstraw P, Crowley J, Chansky K, Giroux DJ, Groome PA, Rami-Porta R, Postmus PE, Rusch V, Sobin L, International Association for the Study of Lung Cancer International Staging C, Participating I. The IASLC Lung Cancer Staging Project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM Classification of malignant tumours. J Thorac Oncol. 2007;2:706–14.CrossRefPubMed
47.
go back to reference Strand TE, Rostad H, Wentzel-Larsen T, von Plessen C. A population-based evaluation of the seventh edition of the TNM system for lung cancer. Eur Respir J. 2010;36:401–7.CrossRefPubMed Strand TE, Rostad H, Wentzel-Larsen T, von Plessen C. A population-based evaluation of the seventh edition of the TNM system for lung cancer. Eur Respir J. 2010;36:401–7.CrossRefPubMed
Metadata
Title
Nomogram integrating gene expression signatures with clinicopathological features to predict survival in operable NSCLC: a pooled analysis of 2164 patients
Authors
Jian Wu
Lizhi Zhou
Lixia Huang
Jincui Gu
Shaoli Li
Baomo Liu
Jinlun Feng
Yanbin Zhou
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Journal of Experimental & Clinical Cancer Research / Issue 1/2017
Electronic ISSN: 1756-9966
DOI
https://doi.org/10.1186/s13046-016-0477-x

Other articles of this Issue 1/2017

Journal of Experimental & Clinical Cancer Research 1/2017 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine