Lung Cancer Screening, Version 3.2018, NCCN Clinical Practice Guidelines in Oncology

Restricted access

Lung cancer is the leading cause of cancer-related mortality in the United States and worldwide. Early detection of lung cancer is an important opportunity for decreasing mortality. Data support using low-dose computed tomography (LDCT) of the chest to screen select patients who are at high risk for lung cancer. Lung screening is covered under the Affordable Care Act for individuals with high-risk factors. The Centers for Medicare & Medicaid Services (CMS) covers annual screening LDCT for appropriate Medicare beneficiaries at high risk for lung cancer if they also receive counseling and participate in shared decision-making before screening. The complete version of the NCCN Guidelines for Lung Cancer Screening provides recommendations for initial and subsequent LDCT screening and provides more detail about LDCT screening. This manuscript focuses on identifying patients at high risk for lung cancer who are candidates for LDCT of the chest and on evaluating initial screening findings.

  • 1.

    Torre LA, Siegel RL, Ward EM, Jemal A. Global cancer incidence and mortality rates and trends—an update. Cancer Epidemiol Biomarkers Prev 2016;25:1627.

    • Search Google Scholar
    • Export Citation
  • 2.

    Torre LA, Bray F, Siegel RL. Global cancer statistics, 2012. CA Cancer J Clin 2015;65:87108.

  • 3.

    The Health Consequences of Smoking: A Report of the Surgeon General (ed 2010/07/30). Atlanta: US Department of Health and Human Services; 2004.

    • Search Google Scholar
    • Export Citation
  • 4.

    Thun MJ, Henley SJ, Burns D. Lung cancer death rates in lifelong nonsmokers. J Natl Cancer Inst 2006;98:691699.

  • 5.

    Jemal A, Bray F, Center MM. Global cancer statistics. CA Cancer J Clin 2011;61:6990.

  • 6.

    Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin 2018;68:730.

  • 7.

    Howlader N, Noone AM, Krapcho M. SEER Cancer Statistics Review, 1975–2014, based on November 2016 SEER data submission, posted to the SEER web site, April 2017. Bethesda, MD: National Cancer Institute; 2017.

    • Search Google Scholar
    • Export Citation
  • 8.

    Jemal A, Ward EM, Johnson CJ. Annual report to the nation on the status of cancer, 1975-2014, featuring survival. J Natl Cancer Inst 2017;109.

  • 9.

    Jemal A, Thun MJ, Ries LA. Annual report to the nation on the status of cancer, 1975-2005, featuring trends in lung cancer, tobacco use, and tobacco control. J Natl Cancer Inst 2008;100:16721694.

    • Search Google Scholar
    • Export Citation
  • 10.

    National Lung Screening Trial Research Team Aberle DR, Berg CD. The National Lung Screening Trial: overview and study design. Radiology 2011;258:243253.

    • Search Google Scholar
    • Export Citation
  • 11.

    National Lung Screening Trial Research Team Aberle DR, Adams AM. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med 2011;365:395409.

    • Search Google Scholar
    • Export Citation
  • 12.

    Aberle DR, DeMello S, Berg CD. Results of the two incidence screenings in the National Lung Screening Trial. N Engl J Med 2013;369:920931.

  • 13.

    National Lung Screening Trial Research Team Church TR, Black WC. Results of initial low-dose computed tomographic screening for lung cancer. N Engl J Med 2013;368:19801991.

    • Search Google Scholar
    • Export Citation
  • 14.

    Kramer BS, Berg CD, Aberle DR, Prorok PC. Lung cancer screening with low-dose helical CT: results from the National Lung Screening Trial (NLST). J Med Screen 2011;18:109111.

    • Search Google Scholar
    • Export Citation
  • 15.

    Midthun DE. Screening for lung cancer. Clin Chest Med 2011;32:659668.

  • 16.

    Moyer VAForce USPST. Screening for lung cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med 2014;160:330338.

    • Search Google Scholar
    • Export Citation
  • 17.

    Detterbeck FC, Mazzone PJ, Naidich DP, Bach PB. Screening for lung cancer: diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest 2013;143:e78S92S.

    • Search Google Scholar
    • Export Citation
  • 18.

    Wood DE, Eapen GA, Ettinger DS. Lung cancer screening. J Natl Compr Canc Netw 2012;10:240265.

  • 19.

    Wood DE. Lung cancer screening: the last 10 years. J Natl Compr Canc Netw 2012;10:13231325.

  • 20.

    Kazerooni EA, Armstrong MR, Amorosa JK. ACR CT accreditation program and the lung cancer screening program designation. J Am Coll Radiol 2016;13:R3034.

    • Search Google Scholar
    • Export Citation
  • 21.

    McKee BJ, Regis SM, McKee AB, Flacke S, Wald C. Performance of ACR Lung-RADS in a clinical CT lung screening program. J Am Coll Radiol 2016;13:R2529.

    • Search Google Scholar
    • Export Citation
  • 22.

    Pinsky PF, Gierada DS, Black W. Performance of Lung-RADS in the National Lung Screening Trial: a retrospective assessment. Ann Intern Med 2015;162:485491.

    • Search Google Scholar
    • Export Citation
  • 23.

    Leone FT, Evers-Casey S, Toll BA, Vachani A. Treatment of tobacco use in lung cancer: Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest 2013;143:e61S77S.

    • Search Google Scholar
    • Export Citation
  • 24.

    Fucito LM, Czabafy S, Hendricks PS. Pairing smoking-cessation services with lung cancer screening: a clinical guideline from the Association for the Treatment of Tobacco Use and Dependence and the Society for Research on Nicotine and Tobacco. Cancer 2016;122:11501159.

    • Search Google Scholar
    • Export Citation
  • 25.

    Sitas F, Weber MF, Egger S, Yap S, Chiew M, O'Connell D. Smoking cessation after cancer. J Clin Oncol 2014;32:35933595.

  • 26.

    Taylor KL, Cox LS, Zincke N, Mehta L, McGuire C, Gelmann E. Lung cancer screening as a teachable moment for smoking cessation. Lung Cancer 2007;56:125134.

    • Search Google Scholar
    • Export Citation
  • 27.

    Cataldo JK, Dubey S, Prochaska JJ. Smoking cessation: an integral part of lung cancer treatment. Oncology 2010;78:289301.

  • 28.

    Hays JT, McFadden DD, Ebbert JO. Pharmacologic agents for tobacco dependence treatment: 2011 update. Curr Atheroscler Rep 2012;14:8592.

  • 29.

    Wiener RS, Gould MK, Arenberg DA. An official American Thoracic Society/American College of Chest Physicians policy statement: implementation of low-dose computed tomography lung cancer screening programs in clinical practice. Am J Respir Crit Care Med 2015;192:881891.

    • Search Google Scholar
    • Export Citation
  • 30.

    Mazzone P, Powell CA, Arenberg D. Components necessary for high-quality lung cancer screening: American College of Chest Physicians and American Thoracic Society Policy Statement. Chest 2015;147:295303.

    • Search Google Scholar
    • Export Citation
  • 31.

    Davis AM, Cifu AS. Lung cancer screening. JAMA 2014;312:12481249.

  • 32.

    Fintelmann FJ, Bernheim A, Digumarthy SR. The 10 pillars of lung cancer screening: rationale and logistics of a lung cancer screening program. Radiographics 2015;35:18931908.

    • Search Google Scholar
    • Export Citation
  • 33.

    Armstrong K, Kim JJ, Halm EA. Using lessons from breast, cervical, and colorectal cancer screening to inform the development of lung cancer screening programs. Cancer 2016;122:13381342.

    • Search Google Scholar
    • Export Citation
  • 34.

    Kazerooni EA, Austin JH, Black WC. ACR-STR practice parameter for the performance and reporting of lung cancer screening thoracic computed tomography (CT): 2014 (Resolution 4). J Thorac Imaging 2014;29:310316.

    • Search Google Scholar
    • Export Citation
  • 35.

    McKee BJ, Regis SM, McKee AB. Performance of ACR Lung-RADS in a clinical CT lung screening program. J Am Coll Radiol 2015;12:273276.

  • 36.

    de Koning HJ, Meza R, Plevritis SK. Benefits and harms of computed tomography lung cancer screening strategies: a comparative modeling study for the U.S. Preventive Services Task Force. Ann Intern Med 2014;160:311320.

    • Search Google Scholar
    • Export Citation
  • 37.

    Wiener RS, Gould MK, Woloshin S. What do you mean, a spot?: A qualitative analysis of patients' reactions to discussions with their physicians about pulmonary nodules. Chest. 2013;143:672677.

    • Search Google Scholar
    • Export Citation
  • 38.

    Aberle DR, Abtin F, Brown K. Computed tomography screening for lung cancer: has it finally arrived? Implications of the national lung screening trial. J Clin Oncol 2013;31:10021008.

    • Search Google Scholar
    • Export Citation
  • 39.

    Goulart BH, Ramsey SD. Moving beyond the national lung screening trial: discussing strategies for implementation of lung cancer screening programs. Oncologist 2013;18:941946.

    • Search Google Scholar
    • Export Citation
  • 40.

    Sox HC. Implementing lung cancer screening under Medicare: the last chance to get it right? JAMA 2014;312:12061207.

  • 41.

    Volk RJ, Hawk E, Bevers TB. Should CMS cover lung cancer screening for the fully informed patient? JAMA 2014;312:11931194.

  • 42.

    Field JK, Smith RA, Aberle DR. International Association for the Study of Lung Cancer Computed Tomography Screening Workshop 2011 report. J Thorac Oncol 2012;7:1019.

    • Search Google Scholar
    • Export Citation
  • 43.

    Bach PB, Mirkin JN, Oliver TK. Benefits and harms of CT screening for lung cancer: a systematic review. JAMA 2012;307:24182429.

  • 44.

    Walter JE, Heuvelmans MA, de Jong PA. Occurrence and lung cancer probability of new solid nodules at incidence screening with low-dose CT: analysis of data from the randomised, controlled NELSON trial. Lancet Oncol 2016;17:907916.

    • Search Google Scholar
    • Export Citation
  • 45.

    Field JK, Duffy SW, Baldwin DR. The UK Lung Cancer Screening Trial: a pilot randomised controlled trial of low-dose computed tomography screening for the early detection of lung cancer. Health Technol Assess 2016;20:1146.

    • Search Google Scholar
    • Export Citation
  • 46.

    Field JK, Duffy SW, Baldwin DR. UK Lung Cancer RCT Pilot Screening Trial: baseline findings from the screening arm provide evidence for the potential implementation of lung cancer screening. Thorax 2016;71:161170.

    • Search Google Scholar
    • Export Citation
  • 47.

    Patz EF Jr., Greco E, Gatsonis C. Lung cancer incidence and mortality in National Lung Screening Trial participants who underwent low-dose CT prevalence screening: a retrospective cohort analysis of a randomised, multicentre, diagnostic screening trial. Lancet Oncol 2016;17:590599.

    • Search Google Scholar
    • Export Citation
  • 48.

    Wille MM, Dirksen A, Ashraf H. Results of the randomized Danish Lung Cancer Screening Trial with focus on high-risk profiling. Am J Respir Crit Care Med 2016;193:542551.

    • Search Google Scholar
    • Export Citation
  • 49.

    Horeweg N, van Rosmalen J, Heuvelmans MA. Lung cancer probability in patients with CT-detected pulmonary nodules: a prespecified analysis of data from the NELSON trial of low-dose CT screening. Lancet Oncol 2014;15:13321341.

    • Search Google Scholar
    • Export Citation
  • 50.

    Horeweg N, Scholten ET, de Jong PA. Detection of lung cancer through low-dose CT screening (NELSON): a prespecified analysis of screening test performance and interval cancers. Lancet Oncol 2014;15:13421350.

    • Search Google Scholar
    • Export Citation
  • 51.

    Prosch H, Schaefer-Prokop C. Screening for lung cancer. Curr Opin Oncol 2014;26:131137.

  • 52.

    Horeweg N, van der Aalst CM, Thunnissen E. Characteristics of lung cancers detected by computer tomography screening in the randomized NELSON trial. Am J Respir Crit Care Med 2013;187:848854.

    • Search Google Scholar
    • Export Citation
  • 53.

    McRonald FE, Yadegarfar G, Baldwin DR. The UK Lung Screen (UKLS): demographic profile of first 88,897 approaches provides recommendations for population screening. Cancer Prev Res (Phila) 2014;7:362371.

    • Search Google Scholar
    • Export Citation
  • 54.

    Field JK, van Klaveren R, Pedersen JH. European randomized lung cancer screening trials: post NLST. J Surg Oncol 2013;108:280286.

  • 55.

    Ru Zhao Y, Xie X, de Koning HJ. NELSON lung cancer screening study. Cancer Imaging 2011;11 Spec No A:S7984.

  • 56.

    Xu DM, Gietema H, de Koning H. Nodule management protocol of the NELSON randomised lung cancer screening trial. Lung Cancer 2006;54:177184.

  • 57.

    Nair A, Hansell DM. European and North American lung cancer screening experience and implications for pulmonary nodule management. Eur Radiol 2011;21:24452454.

    • Search Google Scholar
    • Export Citation
  • 58.

    van Iersel CA, de Koning HJ, Draisma G. Risk-based selection from the general population in a screening trial: selection criteria, recruitment and power for the Dutch-Belgian randomised lung cancer multi-slice CT screening trial (NELSON). Int J Cancer 2007;120:868874.

    • Search Google Scholar
    • Export Citation
  • 59.

    Patz EF Jr., Pinsky P, Gatsonis C. Overdiagnosis in low-dose computed tomography screening for lung cancer. JAMA Intern Med 2014;174:269274.

  • 60.

    Reich JM. A critical appraisal of overdiagnosis: estimates of its magnitude and implications for lung cancer screening. Thorax 2008;63:377383.

    • Search Google Scholar
    • Export Citation
  • 61.

    Black WC. Computed tomography screening for lung cancer: review of screening principles and update on current status. Cancer 2007;110:23702384.

    • Search Google Scholar
    • Export Citation
  • 62.

    Oken MM, Hocking WG, Kvale PA. Screening by chest radiograph and lung cancer mortality: the Prostate, Lung, Colorectal, and Ovarian (PLCO) randomized trial. JAMA 2011;306:18651873.

    • Search Google Scholar
    • Export Citation
  • 63.

    Wender R, Fontham ET, Barrera E Jr.. American Cancer Society lung cancer screening guidelines. CA Cancer J Clin 2013;63:107117.

  • 64.

    Jaklitsch MT, Jacobson FL, Austin JH. The American Association for Thoracic Surgery guidelines for lung cancer screening using low-dose computed tomography scans for lung cancer survivors and other high-risk groups. J Thorac Cardiovasc Surg 2012;144:3338.

    • Search Google Scholar
    • Export Citation
  • 65.

    Roberts H, Walker-Dilks C, Sivjee K. Screening high-risk populations for lung cancer: guideline recommendations. J Thorac Oncol 2013;8:12321237.

    • Search Google Scholar
    • Export Citation
  • 66.

    Alberg AJ, Brock MV, Ford JG. Epidemiology of lung cancer: diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest 2013;143:e1S29S.

    • Search Google Scholar
    • Export Citation
  • 67.

    Driscoll T, Nelson DI, Steenland K. The global burden of disease due to occupational carcinogens. Am J Ind Med 2005;48:419431.

  • 68.

    de Groot P, Munden RF. Lung cancer epidemiology, risk factors, and prevention. Radiol Clin North Am 2012;50:863876.

  • 69.

    Youlden DR, Cramb SM, Baade PD. The international epidemiology of lung cancer: geographical distribution and secular trends. J Thorac Oncol 2008;3:819831.

    • Search Google Scholar
    • Export Citation
  • 70.

    Jamal A, King BA, Neff LJ. Current cigarette smoking among adults - United States, 2005-2015. MMWR Morb Mortal Wkly Rep 2016;65:12051211.

  • 71.

    Jacobs EJ, Newton CC, Carter BD. What proportion of cancer deaths in the contemporary United States is attributable to cigarette smoking? Ann Epidemiol 2015;25:179182 e171.

    • Search Google Scholar
    • Export Citation
  • 72.

    Centers for Disease Control and Prevention. Current cigarette smoking among adults—United States, 2011. MMWR Morb Mortal Wkly Rep 2012;61:889894.

    • Search Google Scholar
    • Export Citation
  • 73.

    Jha P, Peto R. Global effects of smoking, of quitting, and of taxing tobacco. N Engl J Med 2014;370:6068.

  • 74.

    Chen LS, Baker T, Hung RJ. Genetic risk can be decreased: quitting smoking decreases and delays lung cancer for smokers with high and low CHRNA5 risk genotypes - a meta-analysis. EBioMedicine 2016;11:219226.

    • Search Google Scholar
    • Export Citation
  • 75.

    Hecht SS. Tobacco smoke carcinogens and lung cancer. J Natl Cancer Inst 1999;91:11941210.

  • 76.

    Secretan B, Straif K, Baan R. A review of human carcinogens--Part E: tobacco, areca nut, alcohol, coal smoke, and salted fish. Lancet Oncol 2009;10:10331034.

    • Search Google Scholar
    • Export Citation
  • 77.

    Sakoda LC, Loomis MM, Doherty JA. Germ line variation in nucleotide excision repair genes and lung cancer risk in smokers. Int J Mol Epidemiol Genet 2012;3:117.

    • Search Google Scholar
    • Export Citation
  • 78.

    Centers for Disease Control and Prevention. Smoking-attributable mortality, years of potential life lost, and productivity losses--United States, 2000-2004. MMWR Morb Mortal Wkly Rep 2008;57:12261228.

    • Search Google Scholar
    • Export Citation
  • 79.

    Jha P, Ramasundarahettige C, Landsman V. 21st-century hazards of smoking and benefits of cessation in the United States. N Engl J Med 2013;368:341350.

    • Search Google Scholar
    • Export Citation
  • 80.

    Doll R, Peto R, Boreham J, Sutherland I. Mortality in relation to smoking: 50 years' observations on male British doctors. BMJ 2004;328:1519.

  • 81.

    Moolgavkar SH, Holford TR, Levy DT. Impact of reduced tobacco smoking on lung cancer mortality in the United States during 1975-2000. J Natl Cancer Inst 2012;104:541548.

    • Search Google Scholar
    • Export Citation
  • 82.

    Peto R, Darby S, Deo H. Smoking, smoking cessation, and lung cancer in the UK since 1950: combination of national statistics with two case-control studies. BMJ 2000;321:323329.

    • Search Google Scholar
    • Export Citation
  • 83.

    Kasza KA, Ambrose BK, Conway KP. Tobacco-product use by adults and youths in the United States in 2013 and 2014. N Engl J Med 2017;376:342353.

    • Search Google Scholar
    • Export Citation
  • 84.

    Hu SS, Neff L, Agaku IT. Tobacco product use among adults - United States, 2013-2014. MMWR Morb Mortal Wkly Rep 2016;65:685691.

  • 85.

    Office on Smoking and Health (US). The Health Consequences of Involuntary Exposure to Tobacco Smoke: A Report of the Surgeon General (ed 2010/07/30). Atlanta: Centers for Disease Control and Prevention; 2006.

    • Search Google Scholar
    • Export Citation
  • 86.

    Garfinkel L. Time trends in lung cancer mortality among nonsmokers and a note on passive smoking. J Natl Cancer Inst 1981;66:10611066.

    • Search Google Scholar
    • Export Citation
  • 87.

    Hackshaw AK, Law MR, Wald NJ. The accumulated evidence on lung cancer and environmental tobacco smoke. BMJ 1997;315:980988.

  • 88.

    Delva F, Margery J, Laurent F. Medical follow-up of workers exposed to lung carcinogens: French evidence-based and pragmatic recommendations. BMC Public Health 2017;17:191.

    • Search Google Scholar
    • Export Citation
  • 89.

    Straif K, Benbrahim-Tallaa L, Baan R. A review of human carcinogens--part C: metals, arsenic, dusts, and fibres. Lancet Oncol 2009;10:453454.

    • Search Google Scholar
    • Export Citation
  • 90.

    Silverman DT, Samanic CM, Lubin JH. The Diesel Exhaust in Miners study: a nested case-control study of lung cancer and diesel exhaust. J Natl Cancer Inst 2012;104:855868.

    • Search Google Scholar
    • Export Citation
  • 91.

    Nelson DI, Concha-Barrientos M, Driscoll T. The global burden of selected occupational diseases and injury risks: methodology and summary. Am J Ind Med 2005;48:400418.

    • Search Google Scholar
    • Export Citation
  • 92.

    Nurminen M, Karjalainen A. Epidemiologic estimate of the proportion of fatalities related to occupational factors in Finland. Scand J Work Environ Health 2001;27:161213.

    • Search Google Scholar
    • Export Citation
  • 93.

    Steenland K, Loomis D, Shy C, Simonsen N. Review of occupational lung carcinogens. Am J Ind Med 1996;29:474490.

  • 94.

    Markowitz SB, Levin SM, Miller A, Morabia A. Asbestos, asbestosis, smoking, and lung cancer. New findings from the North American insulator cohort. Am J Respir Crit Care Med 2013;188:9096.

    • Search Google Scholar
    • Export Citation
  • 95.

    Frost G, Darnton A, Harding AH. The effect of smoking on the risk of lung cancer mortality for asbestos workers in Great Britain (1971-2005). Ann Occup Hyg 2011;55:239247.

    • Search Google Scholar
    • Export Citation
  • 96.

    Reid A, de Klerk NH, Ambrosini GL. The risk of lung cancer with increasing time since ceasing exposure to asbestos and quitting smoking. Occup Environ Med 2006;63:509512.

    • Search Google Scholar
    • Export Citation
  • 97.

    El Ghissassi F, Baan R, Straif K. A review of human carcinogens--part D: radiation. Lancet Oncol 2009;10:751752.

  • 98.

    Leuraud K, Schnelzer M, Tomasek L. Radon, smoking and lung cancer risk: results of a joint analysis of three European case-control studies among uranium miners. Radiat Res 2011;176:375387.

    • Search Google Scholar
    • Export Citation
  • 99.

    Lubin JH & Boice JD Jr. Lung cancer risk from residential radon: meta-analysis of eight epidemiologic studies. J Natl Cancer Inst 1997;89:4957.

    • Search Google Scholar
    • Export Citation
  • 100.

    Darby S, Hill D, Auvinen A. Radon in homes and risk of lung cancer: collaborative analysis of individual data from 13 European case-control studies. BMJ 2005;330:223.

    • Search Google Scholar
    • Export Citation
  • 101.

    Wu GX, Nelson RA, Kim JY, Raz DJ. Non-small cell lung cancer as a second primary among patients with previous malignancy: who is at risk? Clin Lung Cancer 2017;18:543550.

    • Search Google Scholar
    • Export Citation
  • 102.

    Tucker MA, Murray N, Shaw EG. Second primary cancers related to smoking and treatment of small-cell lung cancer. Lung Cancer Working Cadre. J Natl Cancer Inst 1997;89:17821788.

    • Search Google Scholar
    • Export Citation
  • 103.

    Shiels MS, Gibson T, Sampson J. Cigarette smoking prior to first cancer and risk of second smoking-associated cancers among survivors of bladder, kidney, head and neck, and stage I lung cancers. J Clin Oncol 2014;32:39893995.

    • Search Google Scholar
    • Export Citation
  • 104.

    Travis LB, Gospodarowicz M, Curtis RE. Lung cancer following chemotherapy and radiotherapy for Hodgkin's disease. J Natl Cancer Inst 2002;94:182192.

    • Search Google Scholar
    • Export Citation
  • 105.

    Morris LG, Sikora AG, Patel SG. Second primary cancers after an index head and neck cancer: subsite-specific trends in the era of human papillomavirus-associated oropharyngeal cancer. J Clin Oncol 2011;29:739746.

    • Search Google Scholar
    • Export Citation
  • 106.

    Kawaguchi T, Matsumura A, Iuchi K. Second primary cancers in patients with stage III non-small cell lung cancer successfully treated with chemo-radiotherapy. Jpn J Clin Oncol 2006;36:711.

    • Search Google Scholar
    • Export Citation
  • 107.

    Richardson GE, Tucker MA, Venzon DJ. Smoking cessation after successful treatment of small-cell lung cancer is associated with fewer smoking-related second primary cancers. Ann Intern Med 1993;119:383390.

    • Search Google Scholar
    • Export Citation
  • 108.

    Jonsson S, Thorsteinsdottir U, Gudbjartsson DF. Familial risk of lung carcinoma in the Icelandic population. JAMA 2004;292:29772983.

  • 109.

    Li X, Hemminki K. Familial multiple primary lung cancers: a population-based analysis from Sweden. Lung Cancer 2005;47:301307.

  • 110.

    Matakidou A, Eisen T, Houlston RS. Systematic review of the relationship between family history and lung cancer risk. Br J Cancer 2005;93:825833.

    • Search Google Scholar
    • Export Citation
  • 111.

    Bailey-Wilson JE, Amos CI, Pinney SM. A major lung cancer susceptibility locus maps to chromosome 6q23-25. Am J Hum Genet 2004;75:460474.

  • 112.

    Thorgeirsson TE, Geller F, Sulem P. A variant associated with nicotine dependence, lung cancer and peripheral arterial disease. Nature 2008;452:638642.

    • Search Google Scholar
    • Export Citation
  • 113.

    Hung RJ, McKay JD, Gaborieau V. A susceptibility locus for lung cancer maps to nicotinic acetylcholine receptor subunit genes on 15q25. Nature 2008;452:633637.

    • Search Google Scholar
    • Export Citation
  • 114.

    Amos CI, Wu X, Broderick P. Genome-wide association scan of tag SNPs identifies a susceptibility locus for lung cancer at 15q25.1. Nat Genet 2008;40:616622.

    • Search Google Scholar
    • Export Citation
  • 115.

    Yang IA, Holloway JW, Fong KM. Genetic susceptibility to lung cancer and co-morbidities. J Thorac Dis 2013;5 Suppl 5:S454462.

  • 116.

    Hwang SJ, Cheng LS, Lozano G. Lung cancer risk in germline p53 mutation carriers: association between an inherited cancer predisposition, cigarette smoking, and cancer risk. Hum Genet 2003;113:238243.

    • Search Google Scholar
    • Export Citation
  • 117.

    Sanders BM, Jay M, Draper GJ, Roberts EM. Non-ocular cancer in relatives of retinoblastoma patients. Br J Cancer 1989;60:358365.

  • 118.

    Fletcher O, Easton D, Anderson K. Lifetime risks of common cancers among retinoblastoma survivors. J Natl Cancer Inst 2004;96:357363.

  • 119.

    Mayne ST, Buenconsejo J, Janerich DT. Previous lung disease and risk of lung cancer among men and women nonsmokers. Am J Epidemiol 1999;149:1320.

    • Search Google Scholar
    • Export Citation
  • 120.

    Samet JM, Humble CG, Pathak DR. Personal and family history of respiratory disease and lung cancer risk. Am Rev Respir Dis 1986;134:466470.

  • 121.

    Alavanja MC, Brownson RC, Boice JD Jr., Hock E. Preexisting lung disease and lung cancer among nonsmoking women. Am J Epidemiol 1992;136:623632.

    • Search Google Scholar
    • Export Citation
  • 122.

    Wu-Williams AH, Dai XD, Blot W. Lung cancer among women in north-east China. Br J Cancer 1990;62:982987.

  • 123.

    Gao YT, Blot WJ, Zheng W. Lung cancer among Chinese women. Int J Cancer 1987;40:604609.

  • 124.

    Brenner AV, Wang Z, Kleinerman RA. Previous pulmonary diseases and risk of lung cancer in Gansu Province, China. Int J Epidemiol 2001;30:118124.

    • Search Google Scholar
    • Export Citation
  • 125.

    Skillrud DM, Offord KP, Miller RD. Higher risk of lung cancer in chronic obstructive pulmonary disease: a prospective, matched, controlled study. Ann Intern Med 1986;105:503507.

    • Search Google Scholar
    • Export Citation
  • 126.

    Yang P, Sun Z, Krowka MJ. Alpha1-antitrypsin deficiency carriers, tobacco smoke, chronic obstructive pulmonary disease, and lung cancer risk. Arch Intern Med 2008;168:10971103.

    • Search Google Scholar
    • Export Citation
  • 127.

    Lowry KP, Gazelle GS, Gilmore ME. Personalizing annual lung cancer screening for patients with chronic obstructive pulmonary disease: a decision analysis. Cancer 2015;121:15561562.

    • Search Google Scholar
    • Export Citation
  • 128.

    Young RP, Hopkins RJ. How the genetics of lung cancer may overlap with COPD. Respirology 2011;16:10471055.

  • 129.

    El-Zein RA, Young RP, Hopkins RJ, Etzel CJ. Genetic predisposition to chronic obstructive pulmonary disease and/or lung cancer: important considerations when evaluating risk. Cancer Prev Res (Phila) 2012;5:522527.

    • Search Google Scholar
    • Export Citation
  • 130.

    Koshiol J, Rotunno M, Consonni D. Chronic obstructive pulmonary disease and altered risk of lung cancer in a population-based case-control study. PLoS One 2009;4:e7380.

    • Search Google Scholar
    • Export Citation
  • 131.

    Young RP, Hopkins RJ, Christmas T. COPD prevalence is increased in lung cancer, independent of age, sex and smoking history. Eur Respir J 2009;34:380386.

    • Search Google Scholar
    • Export Citation
  • 132.

    Turner MC, Chen Y, Krewski D. Chronic obstructive pulmonary disease is associated with lung cancer mortality in a prospective study of never smokers. Am J Respir Crit Care Med 2007;176:285290.

    • Search Google Scholar
    • Export Citation
  • 133.

    Turner-Warwick M, Lebowitz M, Burrows B, Johnson A. Cryptogenic fibrosing alveolitis and lung cancer. Thorax 1980;35:496499.

  • 134.

    Hubbard R, Venn A, Lewis S, Britton J. Lung cancer and cryptogenic fibrosing alveolitis: a population-based cohort study. Am J Respir Crit Care Med 2000;161:58.

    • Search Google Scholar
    • Export Citation
  • 135.

    Hughes JM, Weill H. Asbestosis as a precursor of asbestos related lung cancer: results of a prospective mortality study. Br J Ind Med 1991;48:229233.

    • Search Google Scholar
    • Export Citation
  • 136.

    Han SS, Ten Haaf K, Hazelton WD. The impact of overdiagnosis on the selection of efficient lung cancer screening strategies. Int J Cancer 2017;140:24362443.

    • Search Google Scholar
    • Export Citation
  • 137.

    McKee BJ, Hashim JA, French RJ. Experience with a CT screening program for individuals at high risk for developing lung cancer. J Am Coll Radiol 2015;12:192197.

    • Search Google Scholar
    • Export Citation
  • 138.

    Kovalchik SA, Tammemagi M, Berg CD. Targeting of low-dose CT screening according to the risk of lung-cancer death. N Engl J Med 2013;369:245254.

    • Search Google Scholar
    • Export Citation
  • 139.

    Berg CD. Formidable challenges ahead for lung cancer screening. Oncology (Williston Park) 2012;26:182, 185.

  • 140.

    Pinsky PF, Berg CD. Applying the National Lung Screening Trial eligibility criteria to the US population: what percent of the population and of incident lung cancers would be covered? J Med Screen 2012;19:154156.

    • Search Google Scholar
    • Export Citation
  • 141.

    Pinsky PF, Kramer BS. Lung cancer risk and demographic characteristics of current 20-29 pack-year smokers: implications for screening. J Natl Cancer Inst 2015;107.

    • Search Google Scholar
    • Export Citation
  • 142.

    Miller DL, Mayfield WR, Luu TD. Community-based multidisciplinary computed tomography screening program improves lung cancer survival. Ann Thorac Surg 2016;101:18641869.

    • Search Google Scholar
    • Export Citation
  • 143.

    Katki HA, Kovalchik SA, Berg CD. Development and validation of risk models to select ever-smokers for CT lung cancer screening. JAMA 2016;315:23002311.

    • Search Google Scholar
    • Export Citation
  • 144.

    Li K, Husing A, Sookthai D. Selecting high-risk individuals for lung cancer screening: a prospective evaluation of existing risk models and eligibility criteria in the German EPIC cohort. Cancer Prev Res (Phila) 2015;8:777785.

    • Search Google Scholar
    • Export Citation
  • 145.

    Tammemagi MC, Church TR, Hocking WG. Evaluation of the lung cancer risks at which to screen ever- and never-smokers: screening rules applied to the PLCO and NLST cohorts. PLoS Med 2014;11:e1001764.

    • Search Google Scholar
    • Export Citation
  • 146.

    Ten Haaf K, Jeon J, Tammemagi MC. Risk prediction models for selection of lung cancer screening candidates: a retrospective validation study. PLoS Med 2017;14:e1002277.

    • Search Google Scholar
    • Export Citation
  • 147.

    Yousaf-Khan U, van der Aalst C, de Jong PA. Risk stratification based on screening history: the NELSON lung cancer screening study. Thorax 2017;72:819824.

    • Search Google Scholar
    • Export Citation
  • 148.

    Saghir Z, Dirksen A, Ashraf H. CT screening for lung cancer brings forward early disease. The randomised Danish Lung Cancer Screening Trial: status after five annual screening rounds with low-dose CT. Thorax 2012;67:296301.

    • Search Google Scholar
    • Export Citation
  • 149.

    Pedersen JH, Ashraf H, Dirksen A. The Danish randomized lung cancer CT screening trial--overall design and results of the prevalence round. J Thorac Oncol 2009;4:608614.

    • Search Google Scholar
    • Export Citation
  • 150.

    Menezes RJ, Roberts HC, Paul NS. Lung cancer screening using low-dose computed tomography in at-risk individuals: the Toronto experience. Lung Cancer 2010;67:177183.

    • Search Google Scholar
    • Export Citation
  • 151.

    Swensen SJ, Jett JR, Hartman TE. CT screening for lung cancer: five-year prospective experience. Radiology 2005;235:259265.

  • 152.

    Wilson DO, Weissfeld JL, Fuhrman CR. The Pittsburgh Lung Screening Study (PLuSS): outcomes within 3 years of a first computed tomography scan. Am J Respir Crit Care Med 2008;178:956961.

    • Search Google Scholar
    • Export Citation
  • 153.

    Pinsky PF, Gierada DS, Hocking W. National Lung Screening Trial findings by age: Medicare-eligible versus under-65 population. Ann Intern Med 2014;161:627633.

    • Search Google Scholar
    • Export Citation
  • 154.

    Varlotto JM, Decamp MM, Flickinger JC. Would screening for lung cancer benefit 75- to 84-year-old residents of the United States? Front Oncol 2014;4:37.

    • Search Google Scholar
    • Export Citation
  • 155.

    Sox HC. Better evidence about screening for lung cancer. N Engl J Med 2011;365:455457.

  • 156.

    Jett JR, Midthun DE. Screening for lung cancer: for patients at increased risk for lung cancer, it works. Ann Intern Med 2011;155:540542.

    • Search Google Scholar
    • Export Citation
  • 157.

    Berrington de Gonzalez A, Kim KP, Berg CD. Low-dose lung computed tomography screening before age 55: estimates of the mortality reduction required to outweigh the radiation-induced cancer risk. J Med Screen 2008;15:153158.

    • Search Google Scholar
    • Export Citation
  • 158.

    Marshall HM, Bowman RV, Yang IA. Screening for lung cancer with low-dose computed tomography: a review of current status. J Thorac Dis 2013;5 Suppl 5:S524539.

    • Search Google Scholar
    • Export Citation
  • 159.

    Yip R, Henschke CI, Xu DM. Lung cancers manifesting as part-solid nodules in the National Lung Screening Trial. AJR Am J Roentgenol 2017;208:10111021.

    • Search Google Scholar
    • Export Citation
  • 160.

    Gardiner N, Jogai S, Wallis A. The revised lung adenocarcinoma classification-an imaging guide. J Thorac Dis 2014;6:S537546.

  • 161.

    Naidich DP, Bankier AA, MacMahon H. Recommendations for the management of subsolid pulmonary nodules detected at CT: a statement from the Fleischner Society. Radiology 2013;266:304317.

    • Search Google Scholar
    • Export Citation
  • 162.

    Seidelman JL, Myers JL, Quint LE. Incidental, subsolid pulmonary nodules at CT: etiology and management. Cancer Imaging 2013;13:365373.

  • 163.

    Hansell DM, Bankier AA, MacMahon H. Fleischner Society: glossary of terms for thoracic imaging. Radiology 2008;246:697722.

  • 164.

    Travis WD, Asamura H, Bankier AA. The IASLC lung cancer staging project: proposals for coding T categories for subsolid nodules and assessment of tumor size in part-solid tumors in the forthcoming eighth edition of the TNM classification of lung cancer. J Thorac Oncol 2016;11:12041223.

    • Search Google Scholar
    • Export Citation
  • 165.

    Travis WD, Brambilla E, Noguchi M. Diagnosis of lung cancer in small biopsies and cytology: implications of the 2011 International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society classification. Arch Pathol Lab Med 2013;137:668684.

    • Search Google Scholar
    • Export Citation
  • 166.

    Travis WD, Brambilla E, Noguchi M. International association for the study of lung cancer/american thoracic society/european respiratory society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol 2011;6:244285.

    • Search Google Scholar
    • Export Citation
  • 167.

    Kim HY, Shim YM, Lee KS. Persistent pulmonary nodular ground-glass opacity at thin-section CT: histopathologic comparisons. Radiology 2007;245:267275.

    • Search Google Scholar
    • Export Citation
  • 168.

    Yip R, Yankelevitz DF, Hu M. Lung cancer deaths in the National Lung Screening Trial attributed to nonsolid nodules. Radiology 2016;281:589596.

    • Search Google Scholar
    • Export Citation
  • 169.

    Fukui M, Suzuki K, Matsunaga T. Surgical intervention for ground glass dominant lesions: observation or outright resection? Jpn J Clin Oncol 2017:16.

    • Search Google Scholar
    • Export Citation
  • 170.

    Gould MK, Donington J, Lynch WR. Evaluation of individuals with pulmonary nodules: when is it lung cancer? Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest 2013;143:e93S120S.

    • Search Google Scholar
    • Export Citation
  • 171.

    Chang B, Hwang JH, Choi YH. Natural history of pure ground-glass opacity lung nodules detected by low-dose CT scan. Chest 2013;143:172178.

  • 172.

    Lindell RM, Hartman TE, Swensen SJ. Five-year lung cancer screening experience: CT appearance, growth rate, location, and histologic features of 61 lung cancers. Radiology 2007;242:555562.

    • Search Google Scholar
    • Export Citation
  • 173.

    MacMahon H, Austin JH, Gamsu G. Guidelines for management of small pulmonary nodules detected on CT scans: a statement from the Fleischner Society. Radiology 2005;237:395400.

    • Search Google Scholar
    • Export Citation
  • 174.

    Jacobs C, van Rikxoort EM, Murphy K. Computer-aided detection of pulmonary nodules: a comparative study using the public LIDC/IDRI database. Eur Radiol 2016;26:21392147.

    • Search Google Scholar
    • Export Citation
  • 175.

    Zhao Y, de Bock GH, Vliegenthart R. Performance of computer-aided detection of pulmonary nodules in low-dose CT: comparison with double reading by nodule volume. Eur Radiol 2012;22:20762084.

    • Search Google Scholar
    • Export Citation
  • 176.

    Armato SG 3rd, McLennan G, Bidaut L. The Lung Image Database Consortium (LIDC) and Image Database Resource Initiative (IDRI): a completed reference database of lung nodules on CT scans. Med Phys 2011;38:915931.

    • Search Google Scholar
    • Export Citation
  • 177.

    Clark TJ, Flood TF, Maximin ST, Sachs PB. Lung CT screening reporting and data system speed and accuracy are increased with the use of a semiautomated computer application. J Am Coll Radiol 2015;12:f13011306.

    • Search Google Scholar
    • Export Citation
  • 178.

    Jacobs C, van Rikxoort EM, Scholten ET. Solid, part-solid, or non-solid?: classification of pulmonary nodules in low-dose chest computed tomography by a computer-aided diagnosis system. Invest Radiol 2015;50:168173.

    • Search Google Scholar
    • Export Citation
  • 179.

    Valencia R, Denecke T, Lehmkuhl L. Value of axial and coronal maximum intensity projection (MIP) images in the detection of pulmonary nodules by multislice spiral CT: comparison with axial 1-mm and 5-mm slices. Eur Radiol 2006;16:325332.

    • Search Google Scholar
    • Export Citation
  • 180.

    Fischbach F, Knollmann F, Griesshaber V. Detection of pulmonary nodules by multislice computed tomography: improved detection rate with reduced slice thickness. Eur Radiol 2003;13:23782383.

    • Search Google Scholar
    • Export Citation
  • 181.

    Kawel N, Seifert B, Luetolf M, Boehm T. Effect of slab thickness on the CT detection of pulmonary nodules: use of sliding thin-slab maximum intensity projection and volume rendering. AJR Am J Roentgenol 2009;192:13241329.

    • Search Google Scholar
    • Export Citation
  • 182.

    Peloschek P, Sailer J, Weber M. Pulmonary nodules: sensitivity of maximum intensity projection versus that of volume rendering of 3D multidetector CT data. Radiology 2007;243:561569.

    • Search Google Scholar
    • Export Citation
  • 183.

    Park EA, Goo JM, Lee JW. Efficacy of computer-aided detection system and thin-slab maximum intensity projection technique in the detection of pulmonary nodules in patients with resected metastases. Invest Radiol 2009;44:105113.

    • Search Google Scholar
    • Export Citation
  • 184.

    Jankowski A, Martinelli T, Timsit JF. Pulmonary nodule detection on MDCT images: evaluation of diagnostic performance using thin axial images, maximum intensity projections, and computer-assisted detection. Eur Radiol 2007;17:31483156.

    • Search Google Scholar
    • Export Citation
  • 185.

    Rubin GD, Lyo JK, Paik DS. Pulmonary nodules on multi-detector row CT scans: performance comparison of radiologists and computer-aided detection. Radiology 2005;234:274283.

    • Search Google Scholar
    • Export Citation
  • 186.

    Fraioli F, Bertoletti L, Napoli A. Computer-aided detection (CAD) in lung cancer screening at chest MDCT: ROC analysis of CAD versus radiologist performance. J Thorac Imaging 2007;22:241246.

    • Search Google Scholar
    • Export Citation
  • 187.

    Sahiner B, Chan HP, Hadjiiski LM. Effect of CAD on radiologists' detection of lung nodules on thoracic CT scans: analysis of an observer performance study by nodule size. Acad Radiol 2009;16:15181530.

    • Search Google Scholar
    • Export Citation
  • 188.

    Das M, Muhlenbruch G, Heinen S. Performance evaluation of a computer-aided detection algorithm for solid pulmonary nodules in low-dose and standard-dose MDCT chest examinations and its influence on radiologists. Br J Radiol 2008;81:841847.

    • Search Google Scholar
    • Export Citation
  • 189.

    Lee HY, Goo JM, Lee HJ. Usefulness of concurrent reading using thin-section and thick-section CT images in subcentimetre solitary pulmonary nodules. Clin Radiol 2009;64:127132.

    • Search Google Scholar
    • Export Citation
  • 190.

    Kubo T, Lin PJ, Stiller W. Radiation dose reduction in chest CT: a review. AJR Am J Roentgenol 2008;190:335343.

  • 191.

    Lee JY, Chung MJ, Yi CA, Lee KS. Ultra-low-dose MDCT of the chest: influence on automated lung nodule detection. Korean J Radiol 2008;9:95101.

  • 192.

    Funama Y, Awai K, Liu D. Detection of nodules showing ground-glass opacity in the lungs at low-dose multidetector computed tomography: phantom and clinical study. J Comput Assist Tomogr 2009;33:4953.

    • Search Google Scholar
    • Export Citation
  • 193.

    Hein PA, Romano VC, Rogalla P. Linear and volume measurements of pulmonary nodules at different CT dose levels - intrascan and interscan analysis. Rofo 2009;181:2431.

    • Search Google Scholar
    • Export Citation
  • 194.

    van Riel SJ, Sanchez CI, Bankier AA. Observer variability for classification of pulmonary nodules on low-dose CT images and its effect on nodule management. Radiology 2015;277:863871.

    • Search Google Scholar
    • Export Citation
  • 195.

    Ridge CA, Yildirim A, Boiselle PM. Differentiating between subsolid and solid pulmonary nodules at CT: inter- and intraobserver agreement between experienced thoracic radiologists. Radiology 2016;278:888896.

    • Search Google Scholar
    • Export Citation
  • 196.

    Kim H, Park CM, Song YS. Measurement variability of persistent pulmonary subsolid nodules on same-day repeat CT: what is the threshold to determine true nodule growth during follow-up? PLoS One 2016;11:e0148853.

    • Search Google Scholar
    • Export Citation
  • 197.

    Penn A, Ma M, Chou BB. Inter-reader variability when applying the 2013 Fleischner guidelines for potential solitary subsolid lung nodules. Acta Radiol 2015;56:11801186.

    • Search Google Scholar
    • Export Citation
  • 198.

    Pinsky PF, Gierada DS, Nath PH. National lung screening trial: variability in nodule detection rates in chest CT studies. Radiology 2013;268:865873.

    • Search Google Scholar
    • Export Citation
  • 199.

    Singh S, Pinsky P, Fineberg NS. Evaluation of reader variability in the interpretation of follow-up CT scans at lung cancer screening. Radiology 2011;259:263270.

    • Search Google Scholar
    • Export Citation
  • 200.

    Gierada DS, Pilgram TK, Ford M. Lung cancer: interobserver agreement on interpretation of pulmonary findings at low-dose CT screening. Radiology 2008;246:265272.

    • Search Google Scholar
    • Export Citation
  • 201.

    Henschke CI, Boffetta P, Gorlova O. Assessment of lung-cancer mortality reduction from CT Screening. Lung Cancer 2011;71:328332.

  • 202.

    van Klaveren RJ, Oudkerk M, Prokop M. Management of lung nodules detected by volume CT scanning. N Engl J Med 2009;361:22212229.

  • 203.

    Lopes Pegna A, Picozzi G, Mascalchi M. Design, recruitment and baseline results of the ITALUNG trial for lung cancer screening with low-dose CT. Lung Cancer 2009;64:3440.

    • Search Google Scholar
    • Export Citation
  • 204.

    Veronesi G, Bellomi M, Scanagatta P. Difficulties encountered managing nodules detected during a computed tomography lung cancer screening program. J Thorac Cardiovasc Surg 2008;136:611617.

    • Search Google Scholar
    • Export Citation
  • 205.

    Infante M, Cavuto S, Lutman FR. A randomized study of lung cancer screening with spiral computed tomography: three-year results from the DANTE trial. Am J Respir Crit Care Med 2009;180:445453.

    • Search Google Scholar
    • Export Citation
  • 206.

    Swensen SJ, Jett JR, Hartman TE. Lung cancer screening with CT: Mayo Clinic experience. Radiology 2003;226:756761.

  • 207.

    Henschke CI, Yankelevitz DF, Naidich DP. CT screening for lung cancer: suspiciousness of nodules according to size on baseline scans. Radiology 2004;231:164168.

    • Search Google Scholar
    • Export Citation
  • 208.

    Henschke CI, Yankelevitz DF, Miettinen OSInternational Early Lung Cancer Action Program Investigators. Computed tomographic screening for lung cancer: the relationship of disease stage to tumor size. Arch Intern Med 2006;166:321325.

    • Search Google Scholar
    • Export Citation
  • 209.

    International Early Lung Cancer Action Program Investigators Henschke CI, Yankelevitz DF. Survival of patients with stage I lung cancer detected on CT screening. N Engl J Med 2006;355:17631771.

    • Search Google Scholar
    • Export Citation
  • 210.

    Steele JD, Buell P. Asymptomatic solitary pulmonary nodules. Host survival, tumor size, and growth rate. J Thorac Cardiovasc Surg 1973;65:140151.

    • Search Google Scholar
    • Export Citation
  • 211.

    Galante E, Reduzzi D, Gallus G. The growth rate in the interpretation of the natural history of lung cancer. Tumori 1984;70:427432.

  • 212.

    Usuda K, Saito Y, Sagawa M. Tumor doubling time and prognostic assessment of patients with primary lung cancer. Cancer 1994;74:22392244.

  • 213.

    Arai T, Kuroishi T, Saito Y. Tumor doubling time and prognosis in lung cancer patients: evaluation from chest films and clinical follow-up study. Japanese Lung Cancer Screening Research Group. Jpn J Clin Oncol 1994;24:199204.

    • Search Google Scholar
    • Export Citation
  • 214.

    Weiss W, Boucot KR, Cooper DA. The histopathology of bronchogenic carcinoma and its relation to growth rate, metastasis, and prognosis. Cancer 1970;26:965970.

    • Search Google Scholar
    • Export Citation
  • 215.

    Patel VK, Naik SK, Naidich DP. A practical algorithmic approach to the diagnosis and management of solitary pulmonary nodules: part 2: pretest probability and algorithm. Chest 2013;143:840846.

    • Search Google Scholar
    • Export Citation
  • 216.

    Murrmann GB, van Vollenhoven FH, Moodley L. Approach to a solid solitary pulmonary nodule in two different settings-”Common is common, rare is rare”. J Thorac Dis 2014;6:237248.

    • Search Google Scholar
    • Export Citation
  • 217.

    Allen TL, Kendi AT, Mitiek MO, Maddaus MA. Combined contrast-enhanced computed tomography and 18-fluoro-2-deoxy-D-glucose-positron emission tomography in the diagnosis and staging of non-small cell lung cancer. Semin Thorac Cardiovasc Surg 2011;23:4350.

    • Search Google Scholar
    • Export Citation
  • 218.

    Swensen SJ, Viggiano RW, Midthun DE. Lung nodule enhancement at CT: multicenter study. Radiology 2000;214:7380.

  • 219.

    Yi CA, Lee KS, Kim BT. Tissue characterization of solitary pulmonary nodule: comparative study between helical dynamic CT and integrated PET/CT. J Nucl Med 2006;47:443450.

    • Search Google Scholar
    • Export Citation
  • 220.

    Christensen JA, Nathan MA, Mullan BP. Characterization of the solitary pulmonary nodule: 18F-FDG PET versus nodule-enhancement CT. AJR Am J Roentgenol 2006;187:13611367.

    • Search Google Scholar
    • Export Citation
  • 221.

    Schillaci O, Travascio L, Bolacchi F. Accuracy of early and delayed FDG PET-CT and of contrast-enhanced CT in the evaluation of lung nodules: a preliminary study on 30 patients. Radiol Med 2009;114:890906.

    • Search Google Scholar
    • Export Citation
  • 222.

    Bastarrika G, Garcia-Velloso MJ, Lozano MD. Early lung cancer detection using spiral computed tomography and positron emission tomography. Am J Respir Crit Care Med 2005;171:13781383.

    • Search Google Scholar
    • Export Citation
  • 223.

    Sebro R, Aparici CM, Hernandez-Pampaloni M. FDG PET/CT evaluation of pathologically proven pulmonary lesions in an area of high endemic granulomatous disease. Ann Nucl Med 2013;27:400405.

    • Search Google Scholar
    • Export Citation
  • 224.

    Reyes N, Onadeko OO, Luraschi-Monjagatta Mdel C. Positron emission tomography in the evaluation of pulmonary nodules among patients living in a coccidioidal endemic region. Lung 2014;192:589593.

    • Search Google Scholar
    • Export Citation
  • 225.

    Huber H, Hodolic M, Stelzmuller I. Malignant disease as an incidental finding at (1)(8)F-FDG-PET/CT scanning in patients with granulomatous lung disease. Nucl Med Commun 2015;36:430437.

    • Search Google Scholar
    • Export Citation
  • 226.

    McWilliams A, Tammemagi MC, Mayo JR. Probability of cancer in pulmonary nodules detected on first screening CT. N Engl J Med 2013;369:910919.

    • Search Google Scholar
    • Export Citation
  • 227.

    Herder GJ, van Tinteren H, Golding RP. Clinical prediction model to characterize pulmonary nodules: validation and added value of 18F-fluorodeoxyglucose positron emission tomography. Chest 2005;128:24902496.

    • Search Google Scholar
    • Export Citation
  • 228.

    Patel VK, Naik SK, Naidich DP. A practical algorithmic approach to the diagnosis and management of solitary pulmonary nodules: part 1: radiologic characteristics and imaging modalities. Chest 2013;143:825839.

    • Search Google Scholar
    • Export Citation
  • 229.

    Gould MK, Fletcher J, Iannettoni MD. Evaluation of patients with pulmonary nodules: when is it lung cancer?: ACCP evidence-based clinical practice guidelines (2nd edition). Chest 2007;132:108S130S.

    • Search Google Scholar
    • Export Citation
  • 230.

    Madsen PH, Holdgaard PC, Christensen JB, Hoilund-Carlsen PF. Clinical utility of F-18 FDG PET-CT in the initial evaluation of lung cancer. Eur J Nucl Med Mol Imaging 2016;43:20842097.

    • Search Google Scholar
    • Export Citation
  • 231.

    Al-Ameri A, Malhotra P, Thygesen H. Risk of malignancy in pulmonary nodules: a validation study of four prediction models. Lung Cancer 2015;89:2730.

    • Search Google Scholar
    • Export Citation
  • 232.

    Infante M, Cavuto S, Lutman FR. Long-term follow-up results of the DANTE trial, a randomized study of lung cancer screening with spiral computed tomography. Am J Respir Crit Care Med 2015;191:11661175.

    • Search Google Scholar
    • Export Citation
  • 233.

    Gierada DS, Pinsky P, Nath H. Projected outcomes using different nodule sizes to define a positive CT lung cancer screening examination. J Natl Cancer Inst 2014;106.

    • Search Google Scholar
    • Export Citation
  • 234.

    Yip R, Henschke CI, Yankelevitz DF, Smith JP. CT screening for lung cancer: alternative definitions of positive test result based on the National Lung Screening Trial and International Early Lung Cancer Action Program databases. Radiology 2014;273:591596.

    • Search Google Scholar
    • Export Citation
  • 235.

    Wood DE, Kazerooni E, Baum SL. Lung cancer screening, version 1.2015: featured updates to the NCCN Guidelines. J Natl Compr Canc Netw 2015;13:2334; quiz 34.

    • Search Google Scholar
    • Export Citation
  • 236.

    Kazerooni EA, Armstrong MR, Amorosa JK. ACR CT accreditation program and the lung cancer screening program designation. J Am Coll Radiol 2015;12:3842.

    • Search Google Scholar
    • Export Citation
  • 237.

    Henschke CI, Yip R, Yankelevitz DF, Smith JPInternational Early Lung Cancer Action Program Investigators. Definition of a positive test result in computed tomography screening for lung cancer: a cohort study. Ann Intern Med 2013;158:246252.

    • Search Google Scholar
    • Export Citation
  • 238.

    Revel MP, Bissery A, Bienvenu M. Are two-dimensional CT measurements of small noncalcified pulmonary nodules reliable? Radiology 2004;231:453458.

    • Search Google Scholar
    • Export Citation
  • 239.

    Rampinelli C, Origgi D, Bellomi M. Low-dose CT: technique, reading methods and image interpretation. Cancer Imaging 2013;12:548556.

  • 240.

    Donnelly EF. Technical parameters and interpretive issues in screening computed tomography scans for lung cancer. J Thorac Imaging 2012;27:224229.

    • Search Google Scholar
    • Export Citation
  • 241.

    Kozower BD, Larner JM, Detterbeck FC, Jones DR. Special treatment issues in non-small cell lung cancer: diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest 2013;143:e369S399S.

    • Search Google Scholar
    • Export Citation
  • 242.

    Kim H, Park CM, Koh JM. Pulmonary subsolid nodules: what radiologists need to know about the imaging features and management strategy. Diagn Interv Radiol 2014;20:4757.

    • Search Google Scholar
    • Export Citation
  • 243.

    Detterbeck FC. Overdiagnosis during lung cancer screening: is it an overemphasised, underappreciated, or tangential issue? Thorax 2014;69:407408.

    • Search Google Scholar
    • Export Citation
  • 244.

    Rampinelli C, De Marco P, Origgi D. Exposure to low dose computed tomography for lung cancer screening and risk of cancer: secondary analysis of trial data and risk-benefit analysis. BMJ 2017;356:j347.

    • Search Google Scholar
    • Export Citation
  • 245.

    Wiener RS. Balancing the benefits and harms of low-dose computed tomography screening for lung cancer: Medicare's options for coverage. Ann Intern Med 2014;161:445446.

    • Search Google Scholar
    • Export Citation
  • 246.

    Ettinger DS. Lung cancer screening: has its time come? Oncology (Williston Park) 2014;28:342, 448.

  • 247.

    Braillon A. Bronchioalveolar lung cancer: screening and overdiagnosis. J Clin Oncol 2014;32:3575.

  • 248.

    Johnson DH, Schiller JH, Bunn PA. Reply to A. Braillon. J Clin Oncol 2014;32:3575.

  • 249.

    Slatore CG, Sullivan DR, Pappas M, Humphrey LL. Patient-centered outcomes among lung cancer screening recipients with computed tomography: a systematic review. J Thorac Oncol 2014;9:927934.

    • Search Google Scholar
    • Export Citation
  • 250.

    Brawley OW, Flenaugh EL. Low-dose spiral CT screening and evaluation of the solitary pulmonary nodule. Oncology (Williston Park) 2014;28:441446.

    • Search Google Scholar
    • Export Citation
  • 251.

    Ma J, Ward EM, Smith R, Jemal A. Annual number of lung cancer deaths potentially avertable by screening in the United States. Cancer 2013;119:13811385.

    • Search Google Scholar
    • Export Citation
  • 252.

    Goldstraw P, Crowley J, Chansky K. 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;2:706714.

    • Search Google Scholar
    • Export Citation
  • 253.

    Rami-Porta R, Ball D, Crowley J. The IASLC Lung Cancer Staging Project: proposals for the revision of the T descriptors in the forthcoming (seventh) edition of the TNM classification for lung cancer. J Thorac Oncol 2007;2:593602.

    • Search Google Scholar
    • Export Citation
  • 254.

    Amin MB, Greene FL, Edge SB, eds. AJCC Staging Manual, 8th ed. New York: Springer International Publishing; 2017.

  • 255.

    Rami-Porta R, Asamura H, Travis WD, Rusch VW. Lung cancer - major changes in the American Joint Committee on Cancer eighth edition cancer staging manual. CA Cancer J Clin 2017;67:138155.

    • Search Google Scholar
    • Export Citation
  • 256.

    Flieder DB, Vazquez M, Carter D. Pathologic findings of lung tumors diagnosed on baseline CT screening. Am J Surg Pathol 2006;30:606613.

  • 257.

    Hall FM. Identification, biopsy, and treatment of poorly understood premalignant, in situ, and indolent low-grade cancers: are we becoming victims of our own success? Radiology 2010;254:655659.

    • Search Google Scholar
    • Export Citation
  • 258.

    Gareen IF, Duan F, Greco EM. Impact of lung cancer screening results on participant health-related quality of life and state anxiety in the National Lung Screening Trial. Cancer 2014;120:34013409.

    • Search Google Scholar
    • Export Citation
  • 259.

    Mets OM, de Jong PA, Prokop M. Computed tomographic screening for lung cancer: an opportunity to evaluate other diseases. JAMA 2012;308:14331434.

    • Search Google Scholar
    • Export Citation
  • 260.

    Mets OM, Buckens CF, Zanen P. Identification of chronic obstructive pulmonary disease in lung cancer screening computed tomographic scans. JAMA 2011;306:17751781.

    • Search Google Scholar
    • Export Citation
  • 261.

    Jacobs PC, Gondrie MJ, Mali WP. Unrequested information from routine diagnostic chest CT predicts future cardiovascular events. Eur Radiol 2011;21:15771585.

    • Search Google Scholar
    • Export Citation
  • 262.

    Sekikawa A, Curb JD, Edmundowicz D. Coronary artery calcification by computed tomography in epidemiologic research and cardiovascular disease prevention. J Epidemiol 2012;22:188198.

    • Search Google Scholar
    • Export Citation
  • 263.

    Silvestri GA. Screening for lung cancer: it works, but does it really work? Ann Intern Med 2011;155:537539.

  • 264.

    Croswell JM, Baker SG, Marcus PM. Cumulative incidence of false-positive test results in lung cancer screening: a randomized trial. Ann Intern Med 2010;152:505512, W176–580.

    • Search Google Scholar
    • Export Citation
  • 265.

    Diederich S, Wormanns D, Semik M. Screening for early lung cancer with low-dose spiral CT: prevalence in 817 asymptomatic smokers. Radiology 2002;222:773781.

    • Search Google Scholar
    • Export Citation
  • 266.

    Gohagan JK, Marcus PM, Fagerstrom RM. Final results of the Lung Screening Study, a randomized feasibility study of spiral CT versus chest X-ray screening for lung cancer. Lung Cancer 2005;47:915.

    • Search Google Scholar
    • Export Citation
  • 267.

    Henschke CI, McCauley DI, Yankelevitz DF. Early Lung Cancer Action Project: overall design and findings from baseline screening. Lancet 1999;354:999105.

    • Search Google Scholar
    • Export Citation
  • 268.

    Kaneko M, Eguchi K, Ohmatsu H. Peripheral lung cancer: screening and detection with low-dose spiral CT versus radiography. Radiology 1996;201:798802.

    • Search Google Scholar
    • Export Citation
  • 269.

    Wiener RS, Schwartz LM, Woloshin S, Welch HG. Population-based risk for complications after transthoracic needle lung biopsy of a pulmonary nodule: an analysis of discharge records. Ann Intern Med 2011;155:137144.

    • Search Google Scholar
    • Export Citation
  • 270.

    Henschke CI, Yip R, Yankelevitz DF, Miettinen OS. Computed tomography screening for lung cancer: prospects of surviving competing causes of death. Clin Lung Cancer 2006;7:323325.

    • Search Google Scholar
    • Export Citation
  • 271.

    McCunney RJ, Li J. Radiation risks in lung cancer screening programs: a comparison with nuclear industry workers and atomic bomb survivors. Chest 2014;145:618624.

    • Search Google Scholar
    • Export Citation
  • 272.

    Bach PB, Jett JR, Pastorino U. Computed tomography screening and lung cancer outcomes. JAMA 2007;297:953961.

  • 273.

    Bach PB, Cramer LD, Schrag D. The influence of hospital volume on survival after resection for lung cancer. N Engl J Med 2001;345:181188.

  • 274.

    Silvestri GA, Handy J, Lackland D. Specialists achieve better outcomes than generalists for lung cancer surgery. Chest 1998;114:675680.

  • 275.

    Stephan F, Boucheseiche S, Hollande J. Pulmonary complications following lung resection: a comprehensive analysis of incidence and possible risk factors. Chest 2000;118:12631270.

    • Search Google Scholar
    • Export Citation
  • 276.

    Sone S, Takashima S, Li F. Mass screening for lung cancer with mobile spiral computed tomography scanner. Lancet 1998;351:12421245.

  • 277.

    Li F, Sone S, Abe H. Lung cancers missed at low-dose helical CT screening in a general population: comparison of clinical, histopathologic, and imaging findings. Radiology 2002;225:673683.

    • Search Google Scholar
    • Export Citation
  • 278.

    Armato SG 3rd, Li F, Giger ML. Lung cancer: performance of automated lung nodule detection applied to cancers missed in a CT screening program. Radiology 2002;225:685692.

    • Search Google Scholar
    • Export Citation
  • 279.

    DeVita VT Jr., Young RC, Canellos GP. Combination versus single agent chemotherapy: a review of the basis for selection of drug treatment of cancer. Cancer 1975;35:98110.

    • Search Google Scholar
    • Export Citation
  • 280.

    Folkman J. Seminars in Medicine of the Beth Israel Hospital, Boston. Clinical applications of research on angiogenesis. N Engl J Med 1995;333:17571763.

    • Search Google Scholar
    • Export Citation