Lung cancer screening: Clinical practice guidelines in oncology

Lung cancer screening with LDCT is a complex and controversial topic, with inherent risks and benefits. Results from the large, prospective, randomized NLST show that lung cancer screening with LDCT can decrease lung cancer–specific mortality by 20% and even decrease all-cause mortality by 7%.8 The NLST results indicate that to prevent one death from lung cancer, 320 high-risk individuals must be screened with LDCT. However, the NLST findings have not been replicated yet in a separate cohort. Further analysis of the NLST is underway, including comparative effectiveness modeling. The cost-effectiveness and true benefit-to-risk ratio for lung cancer screening still must be determined. At some point, an acceptable level of risk will have to be deemed appropriate for the benefits of screening. The NCCN Lung Cancer Screening Panel recommends helical LDCT screening for select patients at high risk for lung cancer based on the NLST results, nonrandomized studies, and observational data. These guidelines discuss in detail the criteria for determining which patients are at high risk, and the algorithm provides recommendations for evaluating and following-up nodules detected on LDCT screening (e.g., solid and part-solid nodules). Smokers should always be encouraged to quit smoking tobacco (http://www.smokefree.gov/). Programs using behavioral counseling combined with medications that promote smoking cessation (approved by the FDA) can be very useful (see Treating Tobacco Use and Dependence: Quick Reference Guide for Clinicians; http://www.surgeongeneral.gov/tobacco/tobaqrg.htm). When considering lung cancer screening, it is important to have a full understanding of all risks and benefits related to screening with LDCT. As policies for implementing lung screening programs are designed, a focus on multidisciplinary programs (incorporating primary care doctors, pulmonologists, radiologists, thoracic surgeons, medical oncologists, and pathologists) will be helpful to optimize decision-making and minimize interventions for patients with benign lung disease.

[1]  J. Remy,et al.  Chest computed tomography using iterative reconstruction vs filtered back projection (Part 2): image quality of low-dose CT examinations in 80 patients , 2011, European Radiology.

[2]  V. Rusch,et al.  Radiotherapy plus chemotherapy with or without surgical resection for stage III non-small-cell lung cancer: a phase III randomised controlled trial , 2009, The Lancet.

[3]  J. Crowley,et al.  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 , 2007, Journal of thoracic oncology : official publication of the International Association for the Study of Lung Cancer.

[4]  Feng Li,et al.  Long-term follow-up study of a population-based 1996-1998 mass screening programme for lung cancer using mobile low-dose spiral computed tomography. , 2007, Lung cancer.

[5]  H. D. de Koning,et al.  Long-term effects of lung cancer computed tomography screening on health-related quality of life: the NELSON trial , 2010, European Respiratory Journal.

[6]  David Spizarny,et al.  Final results of the Lung Screening Study, a randomized feasibility study of spiral CT versus chest X-ray screening for lung cancer. , 2005, Lung cancer.

[7]  R C Young,et al.  Combination versus single agent chemotherapy: A review of the basis for selection of drug treatment of cancer , 1975, Cancer.

[8]  Carlo Catalano,et al.  Computer-aided Detection (CAD) in Lung Cancer Screening at Chest MDCT: ROC Analysis of CAD Versus Radiologist Performance , 2007, Journal of thoracic imaging.

[9]  S. Swensen,et al.  Relation between smoking cessation and receiving results from three annual spiral chest computed tomography scans for lung carcinoma screening , 2005, Cancer.

[10]  Jared A. Christensen,et al.  Characterization of the solitary pulmonary nodule: 18F-FDG PET versus nodule-enhancement CT. , 2006, AJR. American journal of roentgenology.

[11]  James H Thrall,et al.  Recommendations for additional imaging in radiology reports: multifactorial analysis of 5.9 million examinations. , 2009, Radiology.

[12]  J. Manson,et al.  Oestrogen plus progestin and lung cancer in postmenopausal women (Women's Health Initiative trial): a post-hoc analysis of a randomised controlled trial , 2009, The Lancet.

[13]  D. Lynch,et al.  The National Lung Screening Trial: overview and study design. , 2011, Radiology.

[14]  R. Jain,et al.  Cells shed from tumours show reduced clonogenicity, resistance to apoptosis, and in vivo tumorigenicity , 1999, British Journal of Cancer.

[15]  P. Buell,et al.  Asymptomatic solitary pulmonary nodules. Host survival, tumor size, and growth rate. , 1973, The Journal of thoracic and cardiovascular surgery.

[16]  J. Folkman Seminars in Medicine of the Beth Israel Hospital, Boston. Clinical applications of research on angiogenesis. , 1995, The New England journal of medicine.

[17]  H. D. de Koning,et al.  High affective risk perception is associated with more lung cancer-specific distress in CT screening for lung cancer. , 2008, Lung cancer.

[18]  J. Habbema,et al.  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) , 2007, International journal of cancer.

[19]  Feng Li,et al.  Mass screening for lung cancer with mobile spiral computed tomography scanner , 1998, The Lancet.

[20]  J. Boice,et al.  Preexisting lung disease and lung cancer among nonsmoking women. , 1992, American journal of epidemiology.

[21]  F. Grannis Can we avert the need for pneumonectomy by screening for lung cancer? , 2004, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[22]  L. Tabár,et al.  Swedish two-county trial: impact of mammographic screening on breast cancer mortality during 3 decades. , 2011, Radiology.

[23]  A. Neugut,et al.  Second primary tumors in patients with head and neck squamous cell carcinoma , 1995, Cancer.

[24]  E. Paci,et al.  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; 254:655-659 , 2010 .

[25]  Millennia Foy,et al.  Assessment of lung-cancer mortality reduction from CT Screening. , 2011, Lung cancer.

[26]  S. Teutsch,et al.  Lung Cancer Screening: An Update for the U.S. Preventive Services Task Force , 2004 .

[27]  C. Henschke,et al.  Modeling the mortality reduction due to computed tomography screening for lung cancer , 2011, Cancer.

[28]  Mingzhu Liang,et al.  The outcome differences of CT screening for lung cancer pre and post following an algorithm in Zhuhai, China. , 2011, Lung cancer.

[29]  A. Dirksen,et al.  The Danish Randomized Lung Cancer CT Screening Trial—Overall Design and Results of the Prevalence Round , 2009, Journal of thoracic oncology : official publication of the International Association for the Study of Lung Cancer.

[30]  R. Hubbard,et al.  Lung cancer and cryptogenic fibrosing alveolitis. A population-based cohort study. , 2000, American journal of respiratory and critical care medicine.

[31]  J. Jett,et al.  Commentary: CT screening for lung cancer--caveat emptor. , 2008, The oncologist.

[32]  H. D. de Koning,et al.  Short-term health-related quality of life consequences in a lung cancer CT screening trial (NELSON) , 2009, British Journal of Cancer.

[33]  Eugenio Paci,et al.  Design, recruitment and baseline results of the ITALUNG trial for lung cancer screening with low-dose CT. , 2009, Lung cancer.

[34]  W. Weiss,et al.  The histopathology of bronchogenic carcinoma and its relation to growth rate, metastasis, and prognosis , 1970, Cancer.

[35]  K. Doi,et al.  Malignant versus benign nodules at CT screening for lung cancer: comparison of thin-section CT findings. , 2004, Radiology.

[36]  D. Ettinger,et al.  Multidisciplinary management of lung cancer. , 2004, The New England journal of medicine.

[37]  S. Armato,et al.  Lung cancers missed at low-dose helical CT screening in a general population: comparison of clinical, histopathologic, and imaging findings. , 2002, Radiology.

[38]  K. Steenland,et al.  Review of occupational lung carcinogens. , 1996, American journal of industrial medicine.

[39]  W. Blot,et al.  Lung cancer among women in north-east China. , 1990, British Journal of Cancer.

[40]  M. Lebowitz,et al.  Cryptogenic fibrosing alveolitis and lung cancer. , 1980, Thorax.

[41]  Paolo Vineis,et al.  A susceptibility locus for lung cancer maps to nicotinic acetylcholine receptor subunit genes on 15q25 , 2008, Nature.

[42]  H. Kauczor,et al.  Radiation dose reduction in chest CT: a review. , 2008, AJR. American journal of roentgenology.

[43]  H. Sox Better evidence about screening for lung cancer. , 2011, The New England journal of medicine.

[44]  N J Wald,et al.  The accumulated evidence on lung cancer and environmental tobacco smoke , 1997, BMJ.

[45]  S. Sone,et al.  Presence of local pleural adhesion in CT screening-detected small nodule in the lung periphery suggests noncancerous, inflammatory nature of the lesion. , 2007, Clinical imaging.

[46]  Thomas Boehm,et al.  Effect of slab thickness on the CT detection of pulmonary nodules: use of sliding thin-slab maximum intensity projection and volume rendering. , 2009, AJR. American journal of roentgenology.

[47]  James A Brink,et al.  Managing incidental findings on abdominal CT: white paper of the ACR incidental findings committee. , 2010, Journal of the American College of Radiology : JACR.

[48]  Christopher I. Amos,et al.  Lung cancer risk in germline p53 mutation carriers: association between an inherited cancer predisposition, cigarette smoking, and cancer risk , 2003, Human Genetics.

[49]  Y. Ohno,et al.  Differentiation of malignant and benign pulmonary nodules with quantitative first-pass 320-detector row perfusion CT versus FDG PET/CT. , 2011, Radiology.

[50]  H. Welch,et al.  Overdiagnosis in cancer. , 2010, Journal of the National Cancer Institute.

[51]  T. Naruke,et al.  Tumor doubling time and prognosis in lung cancer patients: evaluation from chest films and clinical follow-up study. Japanese Lung Cancer Screening Research Group. , 1994, Japanese journal of clinical oncology.

[52]  C. Henschke,et al.  Pathologic Findings of Lung Tumors Diagnosed on Baseline CT Screening , 2006, The American journal of surgical pathology.

[53]  C. Henschke,et al.  Comparison of pathologic findings of baseline and annual repeat cancers diagnosed on CT screening. , 2007, Lung cancer.

[54]  Daniel F. Gudbjartsson,et al.  A variant associated with nicotine dependence, lung cancer and peripheral arterial disease , 2008, Nature.

[55]  A. Flahault,et al.  Pulmonary complications following lung resection: a comprehensive analysis of incidence and possible risk factors. , 2000, Chest.

[56]  J. Gohagan,et al.  Cumulative Incidence of False-Positive Results in Repeated, Multimodal Cancer Screening , 2009, The Annals of Family Medicine.

[57]  O. Miettinen,et al.  Survival of Patients with Stage I Lung Cancer Detected on CT Screening , 2008 .

[58]  Frank Fischbach,et al.  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 , 2006, European Radiology.

[59]  Dianna D. Cody,et al.  Estimated radiation dose associated with low-dose chest CT of average-size participants in the National Lung Screening Trial. , 2011, AJR. American journal of roentgenology.

[60]  L. Tanoue,et al.  Cumulative Incidence of False-Positive Test Results in Lung Cancer Screening: A Randomized Trial , 2011 .

[61]  L. Garfinkel Time trends in lung cancer mortality among nonsmokers and a note on passive smoking. , 1981, Journal of the National Cancer Institute.

[62]  M. L. R. D. Christenson Compliance with Fleischner Society guidelines for management of small lung nodules: a survey of 834 radiologists , 2011 .

[63]  D. Easton,et al.  Lifetime risks of common cancers among retinoblastoma survivors. , 2004, Journal of the National Cancer Institute.

[64]  A. Dirksen,et al.  Effect of CT screening on smoking habits at 1-year follow-up in the Danish Lung Cancer Screening Trial (DLCST) , 2008, Thorax.

[65]  M. L. R. D. Christenson,et al.  Guidelines for Management of Small Pulmonary Nodules Detected on CT Scans: A Statement From the Fleischner Society , 2006 .

[66]  K P Offord,et al.  Higher risk of lung cancer in chronic obstructive pulmonary disease. A prospective, matched, controlled study. , 1986, Annals of internal medicine.

[67]  G. Pelosi,et al.  Difficulties encountered managing nodules detected during a computed tomography lung cancer screening program. , 2008, The Journal of thoracic and cardiovascular surgery.

[68]  Byung-Tae Kim,et al.  Tissue characterization of solitary pulmonary nodule: comparative study between helical dynamic CT and integrated PET/CT. , 2006, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[69]  S. Mayne,et al.  Previous lung disease and risk of lung cancer among men and women nonsmokers. , 1999, American journal of epidemiology.

[70]  S. Ou,et al.  Natural history of stage I non-small cell lung cancer: implications for early detection. , 2007, Chest.

[71]  L. Tanoue,et al.  Subsolid Pulmonary Nodules and the Spectrum of Peripheral Adenocarcinomas of the Lung: Recommended Interim Guidelines for Assessment and Management , 2011 .

[72]  M. Revel,et al.  Are two-dimensional CT measurements of small noncalcified pulmonary nodules reliable? , 2004, Radiology.

[73]  F. Grannis,et al.  Cost of a 5-year lung cancer survivor: symptomatic tumour identification vs proactive computed tomography screening , 2009, British Journal of Cancer.

[74]  J. Reich A critical appraisal of overdiagnosis: estimates of its magnitude and implications for lung cancer screening , 2008, Thorax.

[75]  M. Tockman,et al.  Screening for lung cancer with CT: a preliminary cost-effectiveness analysis. , 2002, Chest.

[76]  R W Günther,et al.  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. , 2008, The British journal of radiology.

[77]  C. Cicciò,et al.  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 , 2009, La radiologia medica.

[78]  S. Swensen,et al.  Thoracic surgical operations in patients enrolled in a computed tomographic screening trial. , 2004, The Journal of thoracic and cardiovascular surgery.

[79]  Lubomir M. Hadjiiski,et al.  Effect of CAD on radiologists' detection of lung nodules on thoracic CT scans: analysis of an observer performance study by nodule size. , 2009, Academic radiology.

[80]  O. Miettinen,et al.  Computed tomography screening for lung cancer: prospects of surviving competing causes of death. , 2006, Clinical lung cancer.

[81]  Kurt Straif,et al.  A review of human carcinogens--part D: radiation. , 2009, The Lancet. Oncology.

[82]  L. Tanoue,et al.  CT Screening for Lung Cancer: Suspiciousness of Nodules According to Size on Baseline Scans , 2006 .

[83]  David J Brenner,et al.  Radiation risks potentially associated with low-dose CT screening of adult smokers for lung cancer. , 2004, Radiology.

[84]  J. Samet,et al.  Personal and family history of respiratory disease and lung cancer risk. , 1986, The American review of respiratory disease.

[85]  W. Black Computed tomography screening for lung cancer: Review of screening principles and update on current status , 2007, Cancer.

[86]  T. Eisen,et al.  Systematic review of the relationship between family history and lung cancer risk , 2005, British Journal of Cancer.

[87]  D. Lackland,et al.  Specialists achieve better outcomes than generalists for lung cancer surgery. , 1998, Chest.

[88]  Y. Shim,et al.  Persistent pulmonary nodular ground-glass opacity at thin-section CT: histopathologic comparisons. , 2007, Radiology.

[89]  G. Gallus,et al.  The Growth Rate in the Interpretation of the Natural History of Lung Cancer , 1984, Tumori.

[90]  D. Ettinger,et al.  Second primary cancers related to smoking and treatment of small-cell lung cancer. Lung Cancer Working Cadre. , 1997, Journal of the National Cancer Institute.

[91]  A. Jankowski,et al.  Pulmonary nodule detection on MDCT images: evaluation of diagnostic performance using thin axial images, maximum intensity projections, and computer-assisted detection , 2007, European Radiology.

[92]  Christoph I. Lee,et al.  CT screening for lung cancer: implications on social responsibility. , 2007, AJR. American journal of roentgenology.

[93]  S. Wacholder,et al.  Chronic Obstructive Pulmonary Disease and Altered Risk of Lung Cancer in a Population-Based Case-Control Study , 2009, PloS one.

[94]  M. Chung,et al.  Ultra-Low-Dose MDCT of the Chest: Influence on Automated Lung Nodule Detection , 2008, Korean journal of radiology.

[95]  F. Hall Identification, biopsy, and treatment of poorly understood premalignant, in situ, and indolent low-grade cancers: are we becoming victims of our own success? , 2010, Radiology.

[96]  Michael J Thun,et al.  Lung cancer death rates in lifelong nonsmokers. , 2006, Journal of the National Cancer Institute.

[97]  Giacomo Belli,et al.  Risk-benefit analysis of X-ray exposure associated with lung cancer screening in the Italung-CT trial. , 2006, AJR. American journal of roentgenology.

[98]  C. Begg,et al.  The influence of hospital volume on survival after resection for lung cancer. , 2001, The New England journal of medicine.

[99]  W C Black,et al.  CT screening for lung cancer: not ready for routine practice. , 2001, Radiology.

[100]  John D Boice,et al.  Lung cancer following chemotherapy and radiotherapy for Hodgkin's disease. , 2002, Journal of the National Cancer Institute.

[101]  K. Hemminki,et al.  Familial multiple primary lung cancers: a population-based analysis from Sweden. , 2005, Lung cancer.

[102]  G. Mills,et al.  Genome-wide association scan of tag SNPs identifies a susceptibility locus for lung cancer at 15q25.1 , 2008, Nature Genetics.

[103]  Deborah Imel Nelson,et al.  The global burden of selected occupational diseases and injury risks: Methodology and summary. , 2005, American journal of industrial medicine.

[104]  S. Swensen,et al.  Lung cancer screening with CT: Mayo Clinic experience. , 2003, Radiology.

[105]  W. Heindel,et al.  Screening for early lung cancer with low-dose spiral CT: prevalence in 817 asymptomatic smokers. , 2002, Radiology.

[106]  Xiao-Cheng Wu,et al.  Annual Report to the Nation on the Status of Cancer, 1975–2005, Featuring Trends in Lung Cancer, Tobacco Use, and Tobacco Control , 2008, Journal of the National Cancer Institute.

[107]  A. Jemal,et al.  Global Cancer Statistics , 2011 .

[108]  Armando Santoro,et al.  A randomized study of lung cancer screening with spiral computed tomography: three-year results from the DANTE trial. , 2009, American journal of respiratory and critical care medicine.

[109]  M. Thun,et al.  Chronic obstructive pulmonary disease is associated with lung cancer mortality in a prospective study of never smokers. , 2007, American journal of respiratory and critical care medicine.

[110]  F. Fischbach,et al.  Detection of pulmonary nodules by multislice computed tomography: improved detection rate with reduced slice thickness , 2003, European Radiology.

[111]  W. Bamlet,et al.  Alpha1-antitrypsin deficiency carriers, tobacco smoke, chronic obstructive pulmonary disease, and lung cancer risk. , 2008, Archives of internal medicine.

[112]  D. Gudbjartsson,et al.  Familial risk of lung carcinoma in the Icelandic population. , 2004, JAMA.

[113]  S. Bölükbas,et al.  Management of lung nodules detected by volume CT scanning. , 2010, The New England journal of medicine.

[114]  J. Goo,et al.  Usefulness of concurrent reading using thin-section and thick-section CT images in subcentimetre solitary pulmonary nodules. , 2009, Clinical radiology.

[115]  A. Sakurada,et al.  Tumor doubling time and prognostic assessment of patients with primary lung cancer , 1994, Cancer.

[116]  Steven E Schild,et al.  Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship. , 2008, Mayo Clinic proceedings.

[117]  Akihiko Yoshizawa,et al.  Impact of proposed IASLC/ATS/ERS classification of lung adenocarcinoma: prognostic subgroups and implications for further revision of staging based on analysis of 514 stage I cases , 2011, Modern Pathology.

[118]  Alexander McGregor,et al.  Lung cancer screening using low-dose computed tomography in at-risk individuals: the Toronto experience. , 2010, Lung cancer.

[119]  Richard Doll,et al.  Smoking, smoking cessation, and lung cancer in the UK since 1950: combination of national statistics with two case-control studies , 2000, BMJ : British Medical Journal.

[120]  J. Lubin,et al.  Previous pulmonary diseases and risk of lung cancer in Gansu Province, China. , 2001, International journal of epidemiology.

[121]  Ting-Yim Lee,et al.  Impact of new technologies on dose reduction in CT. , 2010, European journal of radiology.

[122]  M. L. R. D. Christenson Perifissural Nodules Seen at CT Screening for Lung Cancer , 2011 .

[123]  C. Henschke,et al.  The cost-effectiveness of low-dose CT screening for lung cancer: preliminary results of baseline screening. , 2003, Chest.

[124]  A. Jemal,et al.  Cancer statistics, 2011 , 2011, CA: a cancer journal for clinicians.

[125]  Deborah Imel Nelson,et al.  The global burden of disease due to occupational carcinogens. , 2005, American journal of industrial medicine.

[126]  Marc Decramer,et al.  The 15q24/25 susceptibility variant for lung cancer and chronic obstructive pulmonary disease is associated with emphysema. , 2010, American journal of respiratory and critical care medicine.

[127]  Elisabeth Brambilla,et al.  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 , 2007, Journal of thoracic oncology : official publication of the International Association for the Study of Lung Cancer.

[128]  C. Begg,et al.  Computed Tomography Screening and Lung Cancer Outcomes , 2008 .

[129]  M. L. R. D. Christenson,et al.  International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society International Multidisciplinary Classification of Lung Adenocarcinoma , 2012 .

[130]  M. L. R. D. Christenson,et al.  Pulmonary Nodules: Sensitivity of Maximum Intensity Projection versus That of Volume Rendering of 3D Multidetector CT Data , 2008 .

[131]  J. Remy,et al.  Chest computed tomography using iterative reconstruction vs filtered back projection (Part 1): evaluation of image noise reduction in 32 patients , 2011, European Radiology.

[132]  N. Müller,et al.  Lung nodule enhancement at CT: multicenter study. , 2000, Radiology.

[133]  Anthony J. Sherbondy,et al.  Pulmonary nodules on multi-detector row CT scans: performance comparison of radiologists and computer-aided detection. , 2005, Radiology.

[134]  H Weill,et al.  Asbestosis as a precursor of asbestos related lung cancer: results of a prospective mortality study. , 1991, British journal of industrial medicine.

[135]  K. Dasmahapatra,et al.  Lung cancer in patients with head and neck cancer. Incidence and long-term survival. , 1987, American journal of surgery.

[136]  Markku Mikael Nurminen,et al.  Epidemiologic estimate of the proportion of fatalities related to occupational factors in Finland. , 2001, Scandinavian journal of work, environment & health.

[137]  S. Armato,et al.  Lung cancer: performance of automated lung nodule detection applied to cancers missed in a CT screening program. , 2002, Radiology.

[138]  Marshall W. Anderson,et al.  A major lung cancer susceptibility locus maps to chromosome 6q23-25. , 2004, American journal of human genetics.

[139]  L. Tanoue CT Screening for Lung Cancer: Five-year Prospective Experience , 2007 .

[140]  M. Roizen Reduced Lung-Cancer Mortality with Low-Dose Computed Tomographic Screening , 2012 .

[141]  R. Doll,et al.  Radon in homes and risk of lung cancer: collaborative analysis of individual data from 13 European case-control studies , 2004, BMJ : British Medical Journal.

[142]  M. L. R. D. Christenson Smooth or attached solid indeterminate nodules detected at baseline CT screening in the NELSON study: cancer risk during 1 year of follow up , 2010 .

[143]  J. Fraumeni,et al.  Lung cancer among Chinese women , 1987, International journal of cancer.

[144]  M. Tucker,et al.  Smoking Cessation after Successful Treatment of Small-Cell Lung Cancer Is Associated with Fewer Smoking-related Second Primary Cancers , 1993, Annals of Internal Medicine.

[145]  Lisa M. Schwartz,et al.  Population-based risk of complications following transthoracic needle lung biopsy of a pulmonary nodule , 2011 .

[146]  Jeong Won Lee,et al.  Efficacy of Computer-Aided Detection System and Thin-Slab Maximum Intensity Projection Technique in the Detection of Pulmonary Nodules in Patients With Resected Metastases , 2009, Investigative radiology.

[147]  John Eng,et al.  Lung cancer screening with helical computed tomography in older adult smokers: a decision and cost-effectiveness analysis. , 2003, JAMA.

[148]  C. Henschke Early lung cancer action project , 2000, Cancer.

[149]  G. Divine,et al.  The economic impact of false-positive cancer screens. , 2004, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[150]  Harry J de Koning,et al.  Impact of computed tomography screening for lung cancer on participants in a randomized controlled trial (NELSON trial) , 2008, Cancer.

[151]  Denis Tack,et al.  Dose Reduction Strategies for Thoracic Multidetector Computed Tomography: Background, Current Issues, and Recommendations , 2010, Journal of thoracic imaging.

[152]  Paul F. Pinsky,et al.  Evaluation of reader variability in the interpretation of follow-up CT scans at lung cancer screening. , 2011, Radiology.

[153]  V. Dicken,et al.  Linear and Volume Measurements of Pulmonary Nodules at Different CT Dose Levels – Intrascan and Interscan Analysis , 2008, RoFo : Fortschritte auf dem Gebiete der Rontgenstrahlen und der Nuklearmedizin.

[154]  G. Ambrosini,et al.  ceasing exposure to asbestos and quitting smoking The risk of lung cancer with increasing time since , 2006 .

[155]  Zoe Wainer,et al.  Does Lung Adenocarcinoma Subtype Predict Patient Survival?: A Clinicopathologic Study Based on the New International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society International Multidisciplinary Lung Adenocarcinoma Classification , 2011, Journal of thoracic oncology : official publication of the International Association for the Study of Lung Cancer.

[156]  A. Dirksen,et al.  Combined use of positron emission tomography and volume doubling time in lung cancer screening with low-dose CT scanning , 2010, Thorax.

[157]  O. Miettinen,et al.  Computed tomographic screening for lung cancer: the relationship of disease stage to tumor size. , 2006, Archives of internal medicine.

[158]  G. Draper,et al.  Non-ocular cancer in relatives of retinoblastoma patients. , 1989, British Journal of Cancer.

[159]  O. Miettinen,et al.  CT screening for lung cancer: suspiciousness of nodules according to size on baseline scans. , 2004, Radiology.

[160]  Takeshi Nakaura,et al.  Detection of Nodules Showing Ground-Glass Opacity in the Lungs at Low-Dose Multidetector Computed Tomography: Phantom and Clinical Study , 2009, Journal of computer assisted tomography.

[161]  B. Hulka Cancer screening degrees of proof and practical application , 1988, Cancer.

[162]  J. Neuberger,et al.  Lung cancer risk from residential radon: meta-analysis of eight epidemiologic studies. , 1997, Journal of the National Cancer Institute.

[163]  Z. Qing Early Lung Cancer Detection Using Spiral Computed Tomography and Positron Emission Tomography , 2007 .

[164]  M. Kreuzer,et al.  Radon, Smoking and Lung Cancer Risk: Results of a Joint Analysis of Three European Case-Control Studies Among Uranium Miners , 2011, Radiation research.

[165]  M. L. R. D. Christenson,et al.  CT Screening for Lung Cancer: Diagnoses Resulting from the New York Early Lung Cancer Action Project , 2008 .

[166]  David J Sugarbaker,et al.  Surgery for early stage non-small cell lung cancer. , 2003, Seminars in surgical oncology.

[167]  H. Ohmatsu,et al.  Peripheral lung cancer: screening and detection with low-dose spiral CT versus radiography. , 1996, Radiology.

[168]  Kavita Garg,et al.  Lung cancer: interobserver agreement on interpretation of pulmonary findings at low-dose CT screening. , 2008, Radiology.

[169]  L. Cox,et al.  Lung cancer screening as a teachable moment for smoking cessation. , 2007, Lung cancer.

[170]  York Springer,et al.  Ajcc Cancer Staging Manual. 7th Ed. New , 2010 .