Integration of multiple “OMIC” biomarkers: A precision medicine strategy for lung cancer

Lung Cancer

Volumn 107, Issue , 2017, Pages 50-58

  Robles, Ana I ^a   Harris, Curtis C ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Cytokine; Gene expression; Low dose computed tomography; Metabolomics; Methylation; MicroRNA

Indexed keywords

BIOLOGICAL MARKER; CYTOKINE; MESSENGER RNA; MICRORNA; TUMOR MARKER;

AGE; ARTICLE; BIOMICS; CANCER ADJUVANT THERAPY; CANCER IMMUNOTHERAPY; CANCER RISK; COMPUTER ASSISTED TOMOGRAPHY; DNA METHYLATION; EPIDEMIOLOGICAL DATA; GENE EXPRESSION; HIGH RISK PATIENT; HUMAN; LUNG CANCER; LUNG NODULE; METABOLITE; PERSONALIZED MEDICINE; PRIORITY JOURNAL; RECURRENCE RISK; SMOKING; CANCER STAGING; CLINICAL TRIAL (TOPIC); DIAGNOSTIC IMAGING; EARLY CANCER DIAGNOSIS; EPIDEMIOLOGY; LUNG TUMOR; MASS SCREENING; METABOLISM; METABOLOMICS; METHYLATION; NON SMALL CELL LUNG CANCER; PATHOLOGY; PROCEDURES; SURVIVAL RATE; TUMOR RECURRENCE; X-RAY COMPUTED TOMOGRAPHY;

BIOMARKERS, TUMOR; CARCINOMA, NON-SMALL-CELL LUNG; CLINICAL TRIALS AS TOPIC; CYTOKINES; EARLY DETECTION OF CANCER; GENE EXPRESSION; HUMANS; LUNG NEOPLASMS; MASS SCREENING; METABOLOMICS; METHYLATION; MICRORNAS; NEOPLASM RECURRENCE, LOCAL; NEOPLASM STAGING; PRECISION MEDICINE; SMOKING; SURVIVAL RATE; TOMOGRAPHY, X-RAY COMPUTED;

EID: 84985946290     PISSN: 01695002     EISSN: 18728332     Source Type: Journal    
DOI: 10.1016/j.lungcan.2016.06.003     Document Type: Article

References (81)

1. [1] Siegel, R.L., Miller, K.D., Jemal, A., Cancer statistics 2015. CA Cancer J. Clin. 65 (2015), 5–29.
2. [2] Torre, L.A., Siegel, R.L., Jemal, A., Lung cancer statistics. Adv. Exp. Med. Biol. 893 (2016), 1–19.
3. [3] Farhat, F.S., Houhou, W., Targeted therapies in non-small cell lung carcinoma: what have we achieved so far?. Ther. Adv. Med. Oncol. 5 (2013), 249–270.
4. [4] Rizvi, N.A., Hellmann, M.D., Snyder, A., Kvistborg, P., Makarov, V., Havel, J.J., Lee, W., Yuan, J., Wong, P., Ho, T.S., Miller, M.L., Rekhtman, N., Moreira, A.L., Ibrahim, F., Bruggeman, C., Gasmi, B., Zappasodi, R., Maeda, Y., Sander, C., Garon, E.B., Merghoub, T., Wolchok, J.D., Schumacher, T.N., Chan, T.A., Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 348 (2015), 124–128.
5. [5] Department of Health and Human Services, U.S., The Health Consequences of Smoking-50 Years of Progress: A Report of the Surgeon General, US Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion., 2014, Office on Smoking and Health, Atlanta (GA).
6. [6] National Lung Screening Trial Research Team, Aberle, D.R., Adams, A.M., Berg, C.D., Black, W.C., Clapp, J.D., Fagerstrom, R.M., Gareen, I.F., Gatsonis, C., Marcus, P.M., Sicks, J.D., Reduced lung-cancer mortality with low-dose computed tomographic screening. N. Engl. J. Med. 365 (2011), 395–409.
7. [7] Bach, P.B., Mirkin, J.N., Oliver, T.K., Azzoli, C.G., Berry, D.A., Brawley, O.W., Byers, T., Colditz, G.A., Gould, M.K., Jett, J.R., Sabichi, A.L., Smith-Bindman, R., Wood, D.E., Qaseem, A., Detterbeck, F.C., Benefits and harms of CT screening for lung cancer: a systematic review. JAMA 307 (2012), 2418–2429.
8. [8] Wender, R., Fontham, E.T., Barrera, E. Jr., Colditz, G.A., Church, T.R., Ettinger, D.S., Etzioni, R., Flowers, C.R., Gazelle, G.S., Kelsey, D.K., LaMonte, S.J., Michaelson, J.S., Oeffinger, K.C., Shih, Y.C., Sullivan, D.C., Travis, W., Walter, L., Wolf, A.M., Brawley, O.W., Smith, R.A., American cancer society lung cancer screening guidelines. CA. Cancer J. Clin. 63 (2013), 107–117.
9. [9] Deffebach, M.E., Humphrey, L., Lung cancer screening. Surg. Clin. North Am. 95 (2015), 967–978.
10. [10] Decision Memo for Screening for Lung Cancer with Low Dose Computed Tomography (LDCT) (CAG-00439N). Centers for Medicare and Medicaid Services.
11. [11] Doria-Rose, V.P., White, M.C., Klabunde, C.N., Nadel, M.R., Richards, T.B., McNeel, T.S., Rodriguez, J.L., Marcus, P.M., Use of lung cancer screening tests in the United States: results from the 2010 national health interview survey. Cancer Epidemiol. Biomark. Prev. 21 (2012), 1049–1059.
12. [12] Tanner, N.T., Aggarwal, J., Gould, M.K., Kearney, P., Diette, G., Vachani, A., Fang, K.C., Silvestri, G.A., Management of pulmonary nodules by community pulmonologists: a multicenter observational study. Chest 148 (2015), 1405–1414.
13. [13] Schmidt, C., Lung cancer screening poised to expand. J. Natl. Cancer Inst., 107, 2015.
14. [14] National Comprehensive Cancer Network Non–Small-Cell Lung Cancer (Version 4.2014).
15. [15] Chansky, K., Sculier, J.P., Crowley, J.J., Giroux, D., Van Meerbeeck, J., Goldstraw, P., International Staging, C., Participating, I., The international association for the study of lung cancer staging project: prognostic factors and pathologic TNM stage in surgically managed non-small cell lung cancer. J. Thorac. Oncol. 4 (2009), 792–801.
16. [16] Toward Precision Medicine: Building a Knowledge Network for Biomedical Research and a New Taxonomy of Disease. 2011, The National Academies Press, Washington (DC).
17. [17] Collins, F.S., Varmus, H., A new initiative on precision medicine. N. Engl. J. Med. 372 (2015), 793–795.
18. [18] McNeil, C., NCI-MATCH launch highlights new trial design in precision-medicine era. J. Natl. Cancer Inst., 107, 2015.
19. [19] Govindan, R., Mandrekar, S.J., Gerber, D.E., Oxnard, G.R., Dahlberg, S.E., Chaft, J., Malik, S., Mooney, M., Abrams, J.S., Janne, P.A., Gandara, D.R., Ramalingam, S.S., Vokes, E.E., ALCHEMIST trials: a golden opportunity to transform outcomes in early-stage non-small cell lung cancer. Clin. Cancer Res. 21 (2015), 5439–5444.
20. [20] McShane, L.M., Polley, M.Y., Development of omics-based clinical tests for prognosis and therapy selection: the challenge of achieving statistical robustness and clinical utility. Clin. Trials 10 (2013), 653–665.
21. [21] Institute of Medicine, Evolution of Translational Omics: Lessons Learned and the Path Forward. 2012, The National Academies Press, Washington (DC).
22. [22] Hassanein, M., Callison, J.C., Callaway-Lane, C., Aldrich, M.C., Grogan, E.L., Massion, P.P., The state of molecular biomarkers for the early detection of lung cancer. Cancer Prev. Res. (Phila) 5 (2012), 992–1006.
23. [23] Dietrich, D., Kneip, C., Raji, O., Liloglou, T., Seegebarth, A., Schlegel, T., Flemming, N., Rausch, S., Distler, J., Fleischhacker, M., Schmidt, B., Giles, T., Walshaw, M., Warburton, C., Liebenberg, V., Field, J.K., Performance evaluation of the DNA methylation biomarker SHOX2 for the aid in diagnosis of lung cancer based on the analysis of bronchial aspirates. Int. J. Oncol. 40 (2012), 825–832.
24. [24] Kratz, J.R., Mann, M.J., Jablons, D.M., International trial of adjuvant therapy in high risk stage I non-squamous cell carcinoma identified by a 14-gene prognostic signature. Transl. Lung Cancer Res. 2 (2013), 222–225.
25. [25] Hirales Casillas, C.E., Flores Fernandez, J.M., Padilla Camberos, E., Herrera Lopez, E.J., Leal Pacheco, G., Martinez Velazquez, M., Current status of circulating protein biomarkers to aid the early detection of lung cancer. Future Oncol. 10 (2014), 1501–1513.
26. [26] Massion, P.P., Biomarkers to the rescue in a lung nodule epidemic. J. Clin. Oncol. 32 (2014), 725–726.
27. [27] Sozzi, G., Boeri, M., Rossi, M., Verri, C., Suatoni, P., Bravi, F., Roz, L., Conte, D., Grassi, M., Sverzellati, N., Marchiano, A., Negri, E., La Vecchia, C., Pastorino, U., Clinical utility of a plasma-based miRNA signature classifier within computed tomography lung cancer screening: a correlative MILD trial study. J. Clin. Oncol. 32 (2014), 768–773.
28. [28] Mahar, A.L., Compton, C., McShane, L.M., Halabi, S., Asamura, H., Rami-Porta, R., Groome, P.A., Molecular modellers working group of american joint committee on, refining prognosis in lung cancer: a report on the quality and relevance of clinical prognostic tools. J. Thorac. Oncol. 10 (2015), 1576–1589.
29. [29] Zheng, Y., Bueno, R., Commercially available prognostic molecular models in early-stage lung cancer: a review of the pervenio lung RS and myriad myPlan lung cancer tests. Expert Rev. Mol. Diagn. 15 (2015), 589–596.
30. [30] Bueno, R., Hughes, E., Wagner, S., Gutin, A.S., Lanchbury, J.S., Zheng, Y., Archer, M.A., Gustafson, C., Jones, J.T., Rushton, K., Saam, J., Kim, E., Barberis, M., Wistuba, I., Wenstrup, R.J., Wallace, W.A., Hartman, A.R., Harrison, D.J., Validation of a molecular and pathological model for five-year mortality risk in patients with early stage lung adenocarcinoma. J. Thorac. Oncol. 10 (2015), 67–73.
31. [31] Montani, F., Marzi, M.J., Dezi, F., Dama, E., Carletti, R.M., Bonizzi, G., Bertolotti, R., Bellomi, M., Rampinelli, C., Maisonneuve, P., Spaggiari, L., Veronesi, G., Nicassio, F., Di Fiore, P.P., Bianchi, F., miR-test: a blood test for lung cancer early detection. J. Natl. Cancer Inst., 107, 2015, djv063.
32. [32] Vachani, A., Pass, H.I., Rom, W.N., Midthun, D.E., Edell, E.S., Laviolette, M., Li, X.J., Fong, P.Y., Hunsucker, S.W., Hayward, C., Mazzone, P.J., Madtes, D.K., Miller, Y.E., Walker, M.G., Shi, J., Kearney, P., Fang, K.C., Massion, P.P., Validation of a multiprotein plasma classifier to identify benign lung nodules. J. Thorac. Oncol. 10 (2015), 629–637.
33. [33] Vachani, A., Whitney, D.H., Parsons, E.C., Lenburg, M., Ferguson, J.S., Silvestri, G.A., Spira, A., Clinical utility of a bronchial genomic classifier in patients with suspected lung cancer. CHEST, 2016, 10.1016/j.chest.2016.02.636.
34. [34] Enewold, L., Mechanic, L.E., Bowman, E.D., Zheng, Y.L., Yu, Z., Trivers, G., Alberg, A.J., Harris, C.C., Serum concentrations of cytokines and lung cancer survival in African Americans and Caucasians. Cancer Epidemiol. Biomark. Prev. 18 (2009), 215–222.
35. [35] Pine, S.R., Mechanic, L.E., Enewold, L., Chaturvedi, A.K., Katki, H.A., Zheng, Y.L., Bowman, E.D., Engels, E.A., Caporaso, N.E., Harris, C.C., Increased levels of circulating interleukin 6, interleukin 8, C-reactive protein, and risk of lung cancer. J. Natl. Cancer Inst. 103 (2011), 1112–1122.
36. [36] Ryan, B.M., Pine, S.R., Chaturvedi, A.K., Caporaso, N., Harris, C.C., A combined prognostic serum interleukin-8 and interleukin-6 classifier for stage 1 lung cancer in the prostate, lung, colorectal, and ovarian cancer screening trial. J. Thorac. Oncol. 9 (2014), 1494–1503.
37. [37] Pine, S.R., Mechanic, L.E., Enewold, L., Bowman, E.D., Ryan, B.M., Cote, M.L., Wenzlaff, A.S., Loffredo, C.A., Olivo-Marston, S., Chaturvedi, A., Caporaso, N.E., Schwartz, A.G., Harris, C.C., Differential serum cytokine levels and risk of lung cancer between african and european americans. Cancer Epidemiol. Biomark. Prev. 25 (2016), 488–497.
38. [38] Mathe, E.A., Patterson, A.D., Haznadar, M., Manna, S.K., Krausz, K.W., Bowman, E.D., Shields, P.G., Idle, J.R., Smith, P.B., Anami, K., Kazandjian, D.G., Hatzakis, E., Gonzalez, F.J., Harris, C.C., Noninvasive urinary metabolomic profiling identifies diagnostic and prognostic markers in lung cancer. Cancer Res. 74 (2014), 3259–3270.
39. [39] Haznadar, M., Cai, Q., Krausz, K.W., Bowman, E.D., Margono, E., Noro, R., Thompson, M.D., Mathe, E.A., Munro, H.M., Steinwandel, M.D., Gonzalez, F.J., Blot, W.J., Harris, C.C., Urinary metabolite risk biomarkers of lung cancer: a prospective cohort study. Cancer Epidemiol. Biomark. Prev. 25 (2016), 978–986.
40. [40] Subramanian, J., Simon, R., Gene expression-based prognostic signatures in lung cancer: ready for clinical use?. J. Natl. Cancer Inst. 102 (2010), 464–474.
41. [41] Subramanian, J., Simon, R., What should physicians look for in evaluating prognostic gene-expression signatures?. Nat. Rev. Clin. Oncol. 7 (2010), 327–334.
42. [42] Yanaihara, N., Caplen, N., Bowman, E., Seike, M., Kumamoto, K., Yi, M., Stephens, R.M., Okamoto, A., Yokota, J., Tanaka, T., Calin, G.A., Liu, C.G., Croce, C.M., Harris, C.C., Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 9 (2006), 189–198.
43. [43] Saito, M., Schetter, A.J., Mollerup, S., Kohno, T., Skaug, V., Bowman, E.D., Mathe, E.A., Takenoshita, S., Yokota, J., Haugen, A., Harris, C.C., The association of microRNA expression with prognosis and progression in early-stage, non-small cell lung adenocarcinoma: a retrospective analysis of three cohorts. Clin. Cancer Res. 17 (2011), 1875–1882.
44. [44] Akagi, I., Okayama, H., Schetter, A.J., Robles, A.I., Kohno, T., Bowman, E.D., Kazandjian, D., Welsh, J.A., Oue, N., Saito, M., Miyashita, M., Uchida, E., Takizawa, T., Takenoshita, S., Skaug, V., Mollerup, S., Haugen, A., Yokota, J., Harris, C.C., Combination of protein coding and noncoding gene expression as a robust prognostic classifier in stage I lung adenocarcinoma. Cancer Res. 73 (2013), 3821–3832.
45. [45] Okayama, H., Schetter, A.J., Ishigame, T., Robles, A.I., Kohno, T., Yokota, J., Takenoshita, S., Harris, C.C., The expression of four genes as a prognostic classifier for stage I lung adenocarcinoma in 12 independent cohorts. Cancer Epidemiol. Biomark. Prev. 23 (2014), 2884–2894.
46. [46] Robles, A.I., Arai, E., Mathe, E.A., Okayama, H., Schetter, A.J., Brown, D., Petersen, D., Bowman, E.D., Noro, R., Welsh, J.A., Edelman, D.C., Stevenson, H.S., Wang, Y., Tsuchiya, N., Kohno, T., Skaug, V., Mollerup, S., Haugen, A., Meltzer, P.S., Yokota, J., Kanai, Y., Harris, C.C., An integrated prognostic classifier for stage I lung adenocarcinoma based on mRNA, microRNA, and DNA methylation biomarkers. J. Thorac. Oncol. 10 (2015), 1037–1048.
47. [47] Campbell, J.D., Alexandrov, A., Kim, J., Wala, J., Berger, A.H., Pedamallu, C.S., Shukla, S.A., Guo, G., Brooks, A.N., Murray, B.A., Imielinski, M., Hu, X., Ling, S., Akbani, R., Rosenberg, M., Cibulskis, C., Ramachandran, A., Collisson, E.A., Kwiatkowski, D.J., Lawrence, M.S., Weinstein, J.N., Verhaak, R.G., Wu, C.J., Hammerman, P.S., Cherniack, A.D., Getz, G., Cancer Genome Atlas Research, N., Artyomov, M.N., Schreiber, R., Govindan, R., Meyerson, M., Distinct patterns of somatic genome alterations in lung adenocarcinomas and squamous cell carcinomas. Nat. Genet. 48 (2016), 607–616.
48. [48] Cancer genome atlas research network, comprehensive molecular profiling of lung adenocarcinoma. Nature 511 (2014), 543–550.
49. [49] Martini, N., Bains, M.S., Burt, M.E., Zakowski, M.F., McCormack, P., Rusch, V.W., Ginsberg, R.J., Incidence of local recurrence and second primary tumors in resected stage I lung cancer. J. Thorac. Cardiovasc. Surg. 109 (1995), 120–129.
50. [50] Kratz, J.R., He, J., Van Den Eeden, S.K., Zhu, Z.H., Gao, W., Pham, P.T., Mulvihill, M.S., Ziaei, F., Zhang, H., Su, B., Zhi, X., Quesenberry, C.P., Habel, L.A., Deng, Q., Wang, Z., Zhou, J., Li, H., Huang, M.C., Yeh, C.C., Segal, M.R., Ray, M.R., Jones, K.D., Raz, D.J., Xu, Z., Jahan, T.M., Berryman, D., He, B., Mann, M.J., Jablons, D.M., A practical molecular assay to predict survival in resected non-squamous, non-small-cell lung cancer: development and international validation studies. Lancet 379 (2012), 823–832.
51. [51] Kratz, J.R., Tham, P.T., Mulvihill, M.S., Ziaei, F., Ray, M.R., Hurst, J.W., Segal, M.R., Berryman, D.M., Chu, W., He, B., Jablons, D.M., Mann, M.J., Analytical validation of a practical molecular assay prognostic of survival in nonsquamous non-small cell lung cancer. Diagn. Mol. Pathol. 22 (2013), 65–69.
52. [52] Wistuba, I.I., Behrens, C., Lombardi, F., Wagner, S., Fujimoto, J., Raso, M.G., Spaggiari, L., Galetta, D., Riley, R., Hughes, E., Reid, J., Sangale, Z., Swisher, S.G., Kalhor, N., Moran, C.A., Gutin, A., Lanchbury, J.S., Barberis, M., Kim, E.S., Validation of a proliferation-based expression signature as prognostic marker in early stage lung adenocarcinoma. Clin. Cancer Res. 19 (2013), 6261–6271.
53. [53] Warf, M.B., Fosso, P.G., Hughes, E., Perry, M., Brown, K.L., Reid, J.E., Kolquist, K.A., Wagner, S., Gutin, A., Roa, B., Analytical validation of a proliferation-based molecular signature used as a prognostic marker in early stage lung adenocarcinoma. Biomark. Med. 9 (2015), 901–910.
54. [54] Silvestri, G.A., Vachani, A., Whitney, D., Elashoff, M., Porta Smith, K., Ferguson, J.S., Parsons, E., Mitra, N., Brody, J., Lenburg, M.E., Spira, A., Team, A.S., A bronchial genomic classifier for the diagnostic evaluation of lung cancer. N. Engl. J. Med. 373 (2015), 243–251.
55. [55] Boeri, M., Verri, C., Conte, D., Roz, L., Modena, P., Facchinetti, F., Calabro, E., Croce, C.M., Pastorino, U., Sozzi, G., MicroRNA signatures in tissues and plasma predict development and prognosis of computed tomography detected lung cancer. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 3713–3718.
56. [56] Bianchi, F., Nicassio, F., Marzi, M., Belloni, E., Dall'olio, V., Bernard, L., Pelosi, G., Maisonneuve, P., Veronesi, G., Di Fiore, P.P., A serum circulating miRNA diagnostic test to identify asymptomatic high-risk individuals with early stage lung cancer. EMBO Mol. Med. 3 (2011), 495–503.
57. [57] Li, X.J., Hayward, C., Fong, P.Y., Dominguez, M., Hunsucker, S.W., Lee, L.W., McLean, M., Law, S., Butler, H., Schirm, M., Gingras, O., Lamontagne, J., Allard, R., Chelsky, D., Price, N.D., Lam, S., Massion, P.P., Pass, H., Rom, W.N., Vachani, A., Fang, K.C., Hood, L., Kearney, P., A blood-based proteomic classifier for the molecular characterization of pulmonary nodules. Sci. Transl. Med., 5, 2013, 207ra142.
58. [58] Djenidi, F., Adam, J., Goubar, A., Durgeau, A., Meurice, G., de Montpreville, V., Validire, P., Besse, B., Mami-Chouaib, F., CD8 + CD103+ tumor-infiltrating lymphocytes are tumor-specific tissue-resident memory T cells and a prognostic factor for survival in lung cancer patients. J. Immunol. 194 (2015), 3475–3486.
59. [59] Mondal, A.M., Horikawa, I., Pine, S.R., Fujita, K., Morgan, K.M., Vera, E., Mazur, S.J., Appella, E., Vojtesek, B., Blasco, M.A., Lane, D.P., Harris, C.C., p53 isoforms regulate aging- and tumor-associated replicative senescence in T lymphocytes. J. Clin. Invest. 123 (2013), 5247–5257.
60. [60] Garon, E.B., Rizvi, N.A., Hui, R., Leighl, N., Balmanoukian, A.S., Eder, J.P., Patnaik, A., Aggarwal, C., Gubens, M., Horn, L., Carcereny, E., Ahn, M.J., Felip, E., Lee, J.S., Hellmann, M.D., Hamid, O., Goldman, J.W., Soria, J.C., Dolled-Filhart, M., Rutledge, R.Z., Zhang, J., Lunceford, J.K., Rangwala, R., Lubiniecki, G.M., Roach, C., Emancipator, K., Gandhi, L., Investigators, K., Pembrolizumab for the treatment of non-small-cell lung cancer. N. Engl. J. Med. 372 (2015), 2018–2028.
61. [61] Brahmer, J., Reckamp, K.L., Baas, P., Crino, L., Eberhardt, W.E., Poddubskaya, E., Antonia, S., Pluzanski, A., Vokes, E.E., Holgado, E., Waterhouse, D., Ready, N., Gainor, J., Aren Frontera, O., Havel, L., Steins, M., Garassino, M.C., Aerts, J.G., Domine, M., Paz-Ares, L., Reck, M., Baudelet, C., Harbison, C.T., Lestini, B., Spigel, D.R., Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N. Engl. J. Med. 373 (2015), 123–135.
62. [62] Pinsky, P.F., Church, T.R., Izmirlian, G., Kramer, B.S., The national lung screening trial: results stratified by demographics, smoking history, and lung cancer histology. Cancer 119 (2013), 3976–3983.
63. [63] Pesch, B., Kendzia, P., Gustavsson, K.H., Jockel, G., Johnen, H., Pohlabeln, A., Olsson, W., Ahrens, I.M., Gross, I., Bruske, H.E., Wichmann, F., Merletti, L., Richiardi, L., Simonato, C., Fortes, J., Siemiatycki, M.E., Parent, D., Consonni, M.T., Landi, N., Caporaso, D., Zaridze, A., Szeszenia-Dabrowska, P., Rudnai, J., Lissowska, I., Stucker, E., Fabianova, R.S., Dumitru, V., Bencko, L., Foretova, V., Janout, C.M., Rudin, P., Brennan, P., Boffetta, K., Bruning, T., Cigarette smoking and lung cancer–relative risk estimates for the major histological types from a pooled analysis of case-control studies. Int. J. Cancer 131 (2012), 1210–1219.
64. [64] Tammemagi, C.M., Neslund-Dudas, C., Simoff, M., Kvale, P., Impact of comorbidity on lung cancer survival. Int. J. Cancer 103 (2003), 792–802.
65. [65] Noro, R., Walsh, N., Ishigame, T., Shiraishi, K., Robles, A.I., Ryan, B.M., Bowman, E., Welsh, J.A., Schetter, A.J., Skaug, V., Mollerup, S., Haugen, A., Yokota, J., Kohno, T., Harris, C.C., Gene expression classifier for prognosis of early-stage squamous cell carcinoma of the lung. J. Thorac. Oncol. 11 (2016), S38–S39.
66. [66] Brenner, D.R., McLaughlin, J.R., Hung, R.J., Previous lung diseases and lung cancer risk: a systematic review and meta-analysis. PLoS One, 6, 2011, e17479.
67. [67] Vogtmann, E., Goedert, J.J., Epidemiologic studies of the human microbiome and cancer. Br. J. Cancer 114 (2016), 237–242.
68. [68] Human microbiome project consortium, structure, function and diversity of the healthy human microbiome. Nature 486 (2012), 207–214.
69. [69] Hosgood, H.D. 3rd, Sapkota, A.R., Rothman, N., Rohan, T., Hu, W., Xu, J., Vermeulen, R., He, X., White, J.R., Wu, G., Wei, F., Mongodin, E.F., Lan, Q., The potential role of lung microbiota in lung cancer attributed to household coal burning exposures. Environ. Mol. Mutagen. 55 (2014), 643–651.
70. [70] Yan, X., Yang, M., Liu, J., Gao, R., Hu, J., Li, J., Zhang, L., Shi, Y., Guo, H., Cheng, J., Razi, M., Pang, S., Yu, X., Hu, S., Discovery and validation of potential bacterial biomarkers for lung cancer. Am. J. Cancer. Res. 5 (2015), 3111–3122.
71. [71] Kikuchi, T., Hassanein, M., Amann, J.M., Liu, Q., Slebos, R.J., Rahman, S.M., Kaufman, J.M., Zhang, X., Hoeksema, M.D., Harris, B.K., Li, M., Shyr, Y., Gonzalez, A.L., Zimmerman, L.J., Liebler, D.C., Massion, P.P., Carbone, D.P., In-depth proteomic analysis of nonsmall cell lung cancer to discover molecular targets and candidate biomarkers. Mol. Cell. Proteom. 11 (2012), 916–932.
72. [72] Indovina, P., Marcelli, E., Pentimalli, F., Tanganelli, P., Tarro, G., Giordano, A., Mass spectrometry-based proteomics: the road to lung cancer biomarker discovery. Mass Spectrom. Rev. 32 (2013), 129–142.
73. [73] Taguchi, F., Solomon, B., Gregorc, V., Roder, H., Gray, R., Kasahara, K., Nishio, M., Brahmer, J., Spreafico, A., Ludovini, V., Massion, P.P., Dziadziuszko, R., Schiller, J., Grigorieva, J., Tsypin, M., Hunsucker, S.W., Caprioli, R., Duncan, M.W., Hirsch, F.R., Bunn, P.A. Jr., Carbone, D.P., Mass spectrometry to classify non-small-cell lung cancer patients for clinical outcome after treatment with epidermal growth factor receptor tyrosine kinase inhibitors: a multicohort cross-institutional study. J. Natl. Cancer Inst. 99 (2007), 838–846.
74. [74] Gregorc, V., Novello, S., Lazzari, C., Barni, S., Aieta, M., Mencoboni, M., Grossi, F., De Pas, T., de Marinis, F., Bearz, A., Floriani, I., Torri, V., Bulotta, A., Cattaneo, A., Grigorieva, J., Tsypin, M., Roder, J., Doglioni, C., Levra, M.G., Petrelli, F., Foti, S., Vigano, M., Bachi, A., Roder, H., Predictive value of a proteomic signature in patients with non-small-cell lung cancer treated with second-line erlotinib or chemotherapy (PROSE): a biomarker-stratified randomised phase 3 trial. Lancet Oncol. 15 (2014), 713–721.
75. [75] Lambin, P., Rios-Velazquez, E., Leijenaar, R., Carvalho, S., van Stiphout, R.G., Granton, P., Zegers, C.M., Gillies, R., Boellard, R., Dekker, A., Aerts, H.J., Radiomics: extracting more information from medical images using advanced feature analysis. Eur. J. Cancer 48 (2012), 441–446.
76. [76] Gillies, R.J., Kinahan, P.E., Hricak, H., Radiomics images are more than pictures, they are data. Radiology 278 (2016), 563–577.
77. [77] Aerts, H.J., Velazquez, E.R., Leijenaar, R.T., Parmar, C., Grossmann, P., Carvalho, S., Bussink, J., Monshouwer, R., Haibe-Kains, B., Rietveld, D., Hoebers, F., Rietbergen, M.M., Leemans, C.R., Dekker, A., Quackenbush, J., Gillies, R.J., Lambin, P., Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat. Commun., 5, 2014, 4006.
78. [78] Wang, H., Schabath, M.B., Liu, Y., Berglund, A.E., Bloom, G.C., Kim, J., Stringfield, O., Eikman, E.A., Klippenstein, D.L., Heine, J.J., Eschrich, S.A., Ye, Z., Gillies, R.J., Semiquantitative computed tomography characteristics for lung adenocarcinoma and their association with lung cancer survival. Clin. Lung Cancer 16 (2015), e141–163.
79. [79] Maldonado, F., Duan, F., Raghunath, S.M., Rajagopalan, S., Karwoski, R.A., Garg, K., Greco, E., Nath, H., Robb, R.A., Bartholmai, B.J., Peikert, T., Noninvasive computed tomography-based risk stratification of lung adenocarcinomas in the national lung screening trial. Am. J. Respir. Crit. Care Med. 192 (2015), 737–744.
80. [80] Thomas, A., Yognand, B., Sanja, A., Heidi, C., Matthew, S., Yuhua, G., Hua, W., Ronald, W., Robert, G., Pierre, P.M., Radiomic analysis for improved lung cancer prediction of indeterminate pulmonary nodules, D100. Lung cancer screening: lessons learned and yet to be learned. Am. Thorac. Soc., 2015, A6119.
81. [81] Schabath, M.B., Liu, Y., Wang, H., Stringfield, O., Balagurunathan, Y., Garcia, A., Hall, L., Goldgof, D., Gillies, R.J., Diagnostic and predictive quantitative-imaging features in lung cancer screening. J. Thorac. Oncol. 11 (2016), S41–S42.