Screening for Lung Cancer With Low-Dose Computed Tomography: A Systematic Review to Update the U.S. Preventive Services Task Force Recommendation

BACKGROUND Lung cancer is the leading cause of cancer-related death in the United States. Because early-stage lung cancer is associated with lower mortality than late-stage disease, early detection and treatment may be beneficial. PURPOSE To update the 2004 review of screening for lung cancer for the U.S. Preventive Services Task Force, focusing on screening with low-dose computed tomography (LDCT). DATA SOURCES MEDLINE (2000 to 31 May 2013), the Cochrane Central Register of Controlled Trials and Cochrane Database of Systematic Reviews (through the fourth quarter of 2012), Scopus, and reference lists. STUDY SELECTION English-language randomized, controlled trials or cohort studies that evaluated LDCT screening for lung cancer. DATA EXTRACTION One reviewer extracted study data about participants, design, analysis, follow-up, and results, and a second reviewer checked extractions. Two reviewers rated study quality using established criteria. DATA SYNTHESIS Four trials reported results of LDCT screening among patients with smoking exposure. One large good-quality trial reported that screening was associated with significant reductions in lung cancer (20%) and all-cause (6.7%) mortality. Three small European trials showed no benefit of screening. Harms included radiation exposure, overdiagnosis, and a high rate of false-positive findings that typically were resolved with further imaging. Smoking cessation was not affected. Incidental findings were common. LIMITATIONS Three trials were underpowered and of insufficient duration to evaluate screening effectiveness. Overdiagnosis, an important harm of screening, is of uncertain magnitude. No studies reported results in women or minority populations. CONCLUSION Strong evidence shows that LDCT screening can reduce lung cancer and all-cause mortality. The harms associated with screening must be balanced with the benefits. PRIMARY FUNDING SOURCE Agency for Healthcare Research and Quality.

[1]  H. Maeda,et al.  Adenosquamous carcinoma of the lung: surgical results as compared with squamous cell and adenocarcinoma cases. , 2012, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[2]  J. Siegfried.  The Pittsburgh Lung Screening Study (PLuSS): Outcomes , 2008 .

[3]  J. Brodersen,et al.  Psychosocial consequences of allocation to lung cancer screening: a randomised controlled trial , 2012, BMJ Open.

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

[5]  H. D. de Koning,et al.  Informed participation in a randomised controlled trial of computed tomography screening for lung cancer , 2009, European Respiratory Journal.

[6]  U. Morandi,et al.  The prognostic impact of tumor size in resected stage I non-small cell lung cancer: evidence for a two thresholds tumor diameters classification. , 2006, Lung cancer.

[7]  H. D. de Koning,et al.  The impact of a lung cancer computed tomography screening result on smoking abstinence , 2010, European Respiratory Journal.

[8]  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.

[9]  P. Kvale,et al.  Diagnostic procedures after a positive spiral computed tomography lung carcinoma screen , 2005, Cancer.

[10]  C. Miller,et al.  A Clinical Model to Estimate Recurrence Risk in Resected Stage I Non-Small Cell Lung Cancer , 2008, American journal of clinical oncology.

[11]  O. Miettinen,et al.  Women's susceptibility to tobacco carcinogens and survival after diagnosis of lung cancer. , 2006, JAMA.

[12]  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.

[13]  Ugo Pastorino,et al.  Annual or biennial CT screening versus observation in heavy smokers: 5-year results of the MILD trial , 2012, European journal of cancer prevention : the official journal of the European Cancer Prevention Organisation.

[14]  D. Aberle,et al.  Results of initial low-dose computed tomographic screening for lung cancer. , 2013, The New England journal of medicine.

[15]  V M Hawthorne,et al.  Impaired lung function and mortality risk in men and women: findings from the Renfrew and Paisley prospective population study , 1996, BMJ.

[16]  Denise R. Aberle,et al.  Baseline Characteristics of Participants in the Randomized National Lung Screening Trial , 2010, Journal of the National Cancer Institute.

[17]  H. Dienemann,et al.  Randomized study on early detection of lung cancer with MSCT in Germany: study design and results of the first screening round , 2012, Journal of Cancer Research and Clinical Oncology.

[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]  E. Fontham,et al.  Environmental tobacco smoke and lung cancer in nonsmoking women: A multicenter study , 1994 .

[20]  M. L. R. D. Christenson,et al.  Reduced Lung-Cancer Mortality with Low-Dose Computed Tomographic Screening , 2012 .

[21]  John Connett,et al.  The Effects of a Smoking Cessation Intervention on 14.5-Year Mortality , 2005, Annals of Internal Medicine.

[22]  K. Nackaerts,et al.  Complications following lung surgery in the Dutch-Belgian randomized lung cancer screening trial. , 2012, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[23]  Federico Cappuzzo,et al.  Lung cancer screening with spiral CT: baseline results of the randomized DANTE trial. , 2008, Lung cancer.

[24]  R. V. van Klaveren,et al.  Lung cancer screening and smoking abstinence: 2 year follow-up data from the Dutch–Belgian randomised controlled lung cancer screening trial , 2010, Thorax.

[25]  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.

[26]  M. Mascalchi,et al.  Dose exposure in the ITALUNG trial of lung cancer screening with low-dose CT. , 2012, The British journal of radiology.

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

[28]  H. Nelson,et al.  Screening for Breast Cancer: Systematic Evidence Review Update for the U. S. Preventive Services Task Force , 2009 .

[29]  Joe Y. Chang,et al.  Clinical Investigation : Thoracic Cancer Comparative Effectiveness of 5 Treatment Strategies for Early-Stage Non-Small Cell Lung Cancer in the Elderly , 2012 .

[30]  Betty J. Flehinger,et al.  Screening for lung cancer. , 1984, Chest.

[31]  B. Gillespie,et al.  Patterns of absolute risk of lung cancer mortality in former smokers. , 1993, Journal of the National Cancer Institute.

[32]  Tomotaka Sobue,et al.  Survival for clinical stage I lung cancer not surgically treated. Comparison between screen‐detected and symptom‐detected cases , 1992, Cancer.

[33]  David G. Da Vila,et al.  The Etiology of Lung Cancer , 1993 .

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

[35]  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.

[36]  M. Romkes,et al.  Smoking Behavior 1 Year after Computed Tomography Screening for Lung Cancer: Effect of Physician Referral for Abnormal CT Findings , 2009, Cancer Epidemiology, Biomarkers & Prevention.

[37]  J A TAIANA,et al.  [Cancer of the lung]. , 1952, The Journal of the International College of Surgeons.

[38]  M Kimmel,et al.  Screening for lung cancer: The Mayo lung project revisited , 1993, Cancer.

[39]  Harry J de Koning,et al.  Management of lung nodules detected by volume CT scanning. , 2009, The New England journal of medicine.

[40]  David A Lynch,et al.  Lung cancer screening in the randomized Prostate, Lung, Colorectal, and Ovarian (PLCO) Cancer Screening Trial. , 2010, Journal of the National Cancer Institute.

[41]  Dawei Yang.  Estimating overdiagnosis in low-dose computed tomography screening for lung cancer : a cohort study , 2013 .

[42]  E. Miyaoka,et al.  Prognosis of 6644 resected non-small cell lung cancers in Japan: a Japanese lung cancer registry study. , 2005, Lung cancer.

[43]  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.

[44]  D. R. Jones.  Video-Assisted Thoracic Surgery Lobectomy: Experience With 1,100 Cases , 2007 .

[45]  M. Kaminski,et al.  Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy , 2013 .

[46]  M. Okada,et al.  Evolution of surgical outcomes for nonsmall cell lung cancer: time trends in 1465 consecutive patients undergoing complete resection. , 2004, The Annals of thoracic surgery.

[47]  E. Bergstralh,et al.  Extended lung cancer incidence follow-up in the Mayo Lung Project and overdiagnosis. , 2006, Journal of the National Cancer Institute.

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

[49]  Pamela S. Sinicrope,et al.  Perceptions of lung cancer risk and beliefs in screening accuracy of spiral computed tomography among high-risk lung cancer family members. , 2010, Academic radiology.

[50]  David F Yankelevitz,et al.  Definition of a Positive Test Result in Computed Tomography Screening for Lung Cancer , 2013, Annals of Internal Medicine.

[51]  J. Gohagan,et al.  Screening by chest radiograph and lung cancer mortality: the Prostate, Lung, Colorectal, and Ovarian (PLCO) randomized trial. , 2011, JAMA.

[52]  J. Jett.  Current treatment of unresectable lung cancer. , 1993, Mayo Clinic proceedings.

[53]  M. Spitz,et al.  Lung carcinoma in former smokers , 1996, Cancer.

[54]  L. Tanoue.  Baseline Characteristics of Participants in the Randomized National Lung Screening Trial , 2012 .

[55]  David O Wilson,et al.  The Pittsburgh Lung Screening Study (PLuSS): outcomes within 3 years of a first computed tomography scan. , 2008, American journal of respiratory and critical care medicine.

[56]  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.

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

[58]  David F Yankelevitz,et al.  Frequency of coronary artery calcification on low-dose computed tomography screening for lung cancer. , 2006, Clinical imaging.

[59]  T Suzuki,et al.  Sensitivity and specificity of lung cancer screening using chest low-dose computed tomography , 2008, British Journal of Cancer.

[60]  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.

[61]  C. Mulrow,et al.  Current methods of the US Preventive Services Task Force: a review of the process. , 2001, American journal of preventive medicine.

[62]  S. Swanson,et al.  Survival following lobectomy and limited resection for the treatment of stage I non-small cell lung cancer<=1 cm in size: a review of SEER data. , 2011, Chest.

[63]  Ali O. Farooqi,et al.  CT screening for lung cancer Assessing a regimen's diagnostic performance. , 2004, Clinical imaging.

[64]  M. Gould,et al.  When the Average Applies to No One: Personalized Decision Making About Potential Benefits of Lung Cancer Screening , 2012, Annals of Internal Medicine.

[65]  C. Wells,et al.  More lung cancer but better survival. Implications of secular trends in "necropsy surprise" rates. , 1989, Chest.

[66]  Martin Krapcho,et al.  SEER Cancer Statistics Review, 1975–2009 (Vintage 2009 Populations) , 2012 .

[67]  C. Henschke,et al.  Smoking Cessation and Relapse during a Lung Cancer Screening Program , 2009, Cancer Epidemiology, Biomarkers & Prevention.

[68]  Y. Nishiwaki,et al.  Long-term survival and risk factors for recurrence in stage I non-small cell lung cancer patients with tumors up to 3 cm in maximum dimension. , 2010, Chest.

[69]  D. Xu,et al.  Nodule management protocol of the NELSON randomised lung cancer screening trial. , 2006, Lung cancer.

[70]  S. Duffy,et al.  Predictive Accuracy of the Liverpool Lung Project Risk Model for Stratifying Patients for Computed Tomography Screening for Lung Cancer , 2012, Annals of Internal Medicine.

[71]  E. Miyaoka,et al.  Japanese Lung Cancer Registry Study of 11,663 Surgical Cases in 2004: Demographic and Prognosis Changes Over Decade , 2011, Journal of thoracic oncology : official publication of the International Association for the Study of Lung Cancer.

[72]  J. Mulshine,et al.  Lung cancer screening with low-dose computed tomography: a non-invasive diagnostic protocol for baseline lung nodules. , 2008, Lung cancer.

[73]  Ken Kodama,et al.  Radical sublobar resection for small-sized non-small cell lung cancer: a multicenter study. , 2006, The Journal of thoracic and cardiovascular surgery.

[74]  CT-Screening for lung cancer does not increase the use of anxiolytic or antidepressant medication , 2012, BMC Cancer.

[75]  K. Osann,et al.  Lung cancer in women: the importance of smoking, family history of cancer, and medical history of respiratory disease. , 1991, Cancer research.

[76]  R. Doll,et al.  Etiology of lung cancer. , 1950, Advances in cancer research.

[77]  Hiroto Hatabu,et al.  Lung cancer screening, radiation, risks, benefits, and uncertainty. , 2012, JAMA.

[78]  Bernard Maitre,et al.  Screening by Chest Radiograph and Lung Cancer Mortality : The Prostate , Lung , Colorectal , and Ovarian ( PLCO ) Randomized Trial , 2022 .

[79]  S. Swensen,et al.  Change in smoking status after spiral chest computed tomography scan screening , 2003, Cancer.

[80]  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.

[81]  B. Møller,et al.  Survival after resection for primary lung cancer: a population based study of 3211 resected patients , 2006, Thorax.

[82]  Brian A. King,et al.  Current cigarette smoking among adults - United States, 2005-2014. , 2015, MMWR. Morbidity and mortality weekly report.

[83]  C. Gatsonis,et al.  Reduced Lung-Cancer Mortality with Low-Dose Computed Tomographic Screening , 2012 .

[84]  Paul Pinsky,et al.  Baseline findings of a randomized feasibility trial of lung cancer screening with spiral CT scan vs chest radiograph: the Lung Screening Study of the National Cancer Institute. , 2004, Chest.

[85]  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.

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

[87]  A. Schwartz,et al.  Racial differences in cancer risk among relatives of patients with early onset lung cancer. , 2007, Chest.

[88]  G. McVey,et al.  Screening for lung cancer using low dose CT scanning: results of 2 year follow up , 2005, Thorax.

[89]  D. Burns,et al.  Primary prevention, smoking, and smoking cessation , 2000, Cancer.

[90]  G. Byrnes,et al.  Screening for lung cancer. , 2004, The Cochrane database of systematic reviews.

[91]  P. Granone,et al.  Factors predicting poor survival after resection of stage IA non-small cell lung cancer. , 2008, The Journal of thoracic and cardiovascular surgery.

[92]  G. Strauss,et al.  Screening for lung cancer: An evidence-based synthesis. , 1999, Surgical oncology clinics of North America.

[93]  Radiological diagnosis of small pulmonary nodules detected on low‐dose screening computed tomography , 2008, Respirology.

[94]  S. Woolf,et al.  Breast Cancer Screening: A Summary of the Evidence for the U.S. Preventive Services Task Force , 2002, Annals of Internal Medicine.

[95]  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.

[96]  L. Humphrey,et al.  Screening for Lung Cancer: Systematic Review to Update the U.S. Preventive Services Task Force Recommendation , 2013 .

[97]  K. Katsouyanni,et al.  Active and passive smoking and pathological indicators of lung cancer risk in an autopsy study. , 1992, JAMA.

[98]  U. P. S. T. Force.  Lung Cancer Screening: Recommendation Statement , 2004, Annals of Internal Medicine.

[99]  T. Naruke,et al.  Survival for clinical stage I lung cancer not surgically treated. Comparison between screen‐detected and symptom‐detected cases , 1992, Cancer.

[100]  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.

[101]  Ravi Menezes,et al.  CT screening for lung cancer: implication of lung biopsy recommendations. , 2012, AJR. American journal of roentgenology.

[102]  R. Mckenna,et al.  Video-assisted thoracic surgery lobectomy: experience with 1,100 cases. , 2006, The Annals of thoracic surgery.

[103]  Anne-Marie Sykes,et al.  CT screening for lung cancer: five-year prospective experience. , 2005, Radiology.

[104]  M. L. R. D. Christenson,et al.  Survival of Patients with Stage I Lung Cancer Detected on CT Screening , 2007 .

[105]  D. Midthun,et al.  Predictive Accuracy of the Liverpool Lung Project Risk Model , 2013, Annals of Internal Medicine.

[106]  D. Berry,et al.  Benefits and harms of CT screening for lung cancer: a systematic review. , 2012, JAMA.

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

[108]  A. Dirksen,et al.  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 , 2012, Thorax.

[109]  J. Weissfeld,et al.  Anxiety, Fear of Cancer, and Perceived Risk of Cancer following Lung Cancer Screening , 2008, Medical decision making : an international journal of the Society for Medical Decision Making.