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Lung cancer screening makes the GRADE
YPMED-04655; No of Pages 2 Preventive Medicine xxx (2016) xxx–xxx
Contents lists available at ScienceDirect
Preventive Medicine journal homepage: www.elsevier.com/locate/ypmed
Editorial
Lung cancer screening makes the GRADE
Article: Screening for lung cancer: A systematic review and metaanalysis Authors: Ali M U, Miller J, Peirson L et al. Lung cancer mortality, when age-adjusted, is falling in Canada and the United States as a consequence of dissemination of effective antismoking efforts (Jemal et al., 2010). None-the-less it remains the leading cause of cancer death in males and females. Therapies, particularly targeted ones, are now making inroads in the dismal survival statistics. An important advance came with the definitive demonstration, now almost four years ago, in the National Lung Screening Trial (NLST) that three annual rounds of low-dose helical computerized tomography (LDCT) compared to chest-X-ray (CXR) lowered lung cancer mortality by 20.0% at 6.5 years (The National Lung Screening Trial Research Team, 2011). The Prostate, Lung, Colorectal and Ovarian Cancer Screening Trial (PLCO) results on CXR screening showed no benefit of CXR screening and lung cancer mortality results for CXR screening for a high-risk group in the PLCO that matched NLST criteria were comparable (Oken et al., 2011). As the NLST was the first randomized clinical trial (RCT) documenting a mortality reduction with screening for lung cancer, a public health challenge emerged. What recommendations for screening would be reasonable in the country or region in which it would be implemented? Specifically, which individuals at high-risk for lung cancer in which the benefits outweigh the harms would undergo screening and given the complexity how could this be achieved in the most cost-effective manner? In the United States, the United States Preventive Services Task Force (USPSTF) and the Centers for Medicare and Medicaid Services (CMS) recommended screening along the NLST criteria of ages 55–74, 30 pack years of smoking and if quit having quit within 15 years but extending the age to 80 and 77 respectively (Moyer, 2014; Centers for Medicare and Medicaid Services). In this issue, Ali and colleagues, from McMaster University and many with the McMaster Evidence Review and Synthesis Center evaluated the published literature on CXR, sputum cytology and LDCT screening for lung cancer to inform the Canadian Task Force on Preventive Health Care (CTFPHC) lung cancer screening guidelines (Ali et al., 2016). These guidelines have been released (Anon, 2016). The guidelines call for lung cancer screening in Canada to be in individuals who meet the NLST entry criteria. Currently, only three annual screens are recommended. The systematic review by Ali et al. includes literature published since the last review for the CTPHC which was performed in 2003. The only RCT results of helical CT screening published have been since then, as were the PLCO results. For the review of the quality of the evidence the Grading of Recommendations, Assessment, Development, and Evaluation (GRADE) system was applied. To my knowledge no other group
evaluating LDCT screening has applied this approach. It is a thorough approach that evaluates methodologic quality, statistical heterogeneity, directness of the body of evidence to the populations of interest, precision and reporting bias. Importantly it also considers the metric of whether or not further research would affect the estimate of effect. To date, only four studies of LDCT have been published, the NLST, Detection and Screening of Early Lung Cancer by Novel Imaging and Molecular Essays Trial (DANTE), Multi-centric Italian Lung Detection Trial (MILD) and Danish Lung Cancer Screening Trail (DLCST). (reviewed in Marshall, 2013) When evaluating DANTE, MILD and DLCST, Ali et al. correctly note that these trials are affected by very small sample size, entry criteria not focused on a consistently high risk group, variable screening intervals and in some cases short follow-up and were therefore rated as low quality. By contrast, the NLST has a large sample size, three rounds of annual screening and clear stopping rules to ensure that trial cessation and releasing of results occurred only when a statistically significant boundary was crossed. For full disclosure, I was the National Cancer Institute — United States Project Officer for the NLST. There remain several small trials, the United Kingdom Lung Cancer Screening Trial (UKLS), German Lung Cancer Screening Intervention Trial (LUSI) and ITALUNG and one moderately sized study Nederlands-Leuvens Longkanker Screenings Ondersoek Trial (NELSON) still to report (Marshall et al., 2013). The GRADE assessment by Ali et al. afforded the quality of the evidence from the NLST a “high” level meaning that it is very unlikely to have the evidence of effect overturned by additional research. In the interests of public health, Ali et al. rightly conclude that screening should be recommended. Many issues remain including which high risk groups to screen to maximize lives saved, definition and evaluation of positive screens to achieve high sensitivity with a specificity that limits false-positives and their attendant evaluation costs and harms from invasive procedures and frequency and duration of screening. Not all questions germane to lung cancer screening or many medical decisions for that matter, can be answered through clinical trials nor through innumerable reviews and meta-analyses of them. Ali et al. chose not to review any individualized risk assessment approaches or modeling. The Cancer Intervention and Surveillance Modeling Network (CISNET) modeling that informed the USPSTF recommendations employed micro-simulation natural history of lung cancer models (De Koning et al., 2014). Data from the NLST and PLCO were available to all of the modelers. Scenarios by grouped characteristics, age of starting, stopping, pack-years and quit duration and screening frequency, annual, biannual and triannual were assessed. A strategy similar to NLST entry criteria with age extending to 80 and continued annual screening beyond three years was judged to balance number of screens with lives saved. The recommendations by the CTFPHC extend only to three
http://dx.doi.org/10.1016/j.ypmed.2016.06.006 0091-7435/© 2016 Published by Elsevier Inc.
Please cite this article as: Berg, C.D., Lung cancer screening makes the GRADE, Prev. Med. (2016), http://dx.doi.org/10.1016/j.ypmed.2016.06.006
2
Editorial
annual rounds. It is unclear what is to occur then, as it is unlikely that over the next few years, screening programs will have been in existence long enough to generate adequate data about long term screening. Ali et al. did not address this issue. Other risk-based models have been developed utilizing individual level data and additional risk factors such as emphysema and family history, to estimate screening benefit based upon this individual risk. In two models one for lung cancer incidence and the other for lung cancer death, the lowest risk participants in the NLST benefited little or not all from screening (Tammemägi et al., 2013; Kovalchik et al., 2013). The lung cancer incidence model was applied to the PLCO showing that high risk individuals both within USPSTF and outside of USPSTF criteria would merit screening and that for the same numbers of individuals screened more lives would be saved by applying the incidence model for screening selection (Tammemagi et al., 2014a). A revised individual risk-based lung cancer death model was validated in the 1997–2001 National Health Interview Survey (NHIS) and then screening effect was projected in a more contemporary 2010–2012 NHIS dataset (Katki et al., 2016). This model was also more efficient than the USPSTF criteria. Those individuals at high risk outside the USPSTF criteria were preferentially African-American, current light smokers particularly women and heavy long-term smokers who had quit more than 15 years prior to risk assessment. Subsequent reviews and guideline development groups such as those that inform the USPSTF and the CTFPHC should look beyond randomized clinical trial data to encompass this information from risk-based models and also information that emerges from carefully conducted screening programs. Ali et al. used RCTs for harm assessment but also used quantitative designs. The harms of screening result primarily from evaluation of the positive examinations. In the NLST there was a high positive rate (24% per screen on average and 39% cumulative after three rounds) most of which (96%) were false-positives. Most follow-up was either clinical or imaging. Invasive testing to rule-out malignancy was also done. Ali et al. point out that death within 60 days of a positive examination was uncommon, only 1.5% in those undergoing invasive evaluation and 0.061% in all of those screened contrasting very favorably with the 6% decrease in all-cause mortality. Other quantitative data was similar. In the United States the American College of Radiology (ACR) has developed Lung-RADS and Manos E, et al., in Canada, LU-RADS to better classify screening LDCT results and aid in evaluation to lower the burden of positive screens (Anon; Manos et al., 2014). However, Pinsky et al. compared Lung-RADS to the NLST retrospectively and noted that while specificity was improved sensitivity suffered (Pinsky et al., 2015). It is unknown as to the clinical effect this will have and with further data emerging from screening programs modification of LungRADS and LU-RADS may be necessary. It is possible that a frequency other than annual screening may be reasonable for some individuals, particularly those with negative screens at baseline. Patz et al. retrospectively analyzed NLST data and showed that the risk of lung cancer was lower in those with a negative screen at baseline (Patz et al., 2016). If this can be confirmed in additional data sets, perhaps with demographic information that allows individualized risk assessment also, the personal and financial burden of screening may be reduced. Ali et al. reviewed two smoking cessation studies from NELSON and DLSCT. The NLST also has data of interest which they did not consider. Participants in the Lung Screening Study portion of the NLST were evaluated for smoking cessation and results analyzed by findings on LDCT and those with more abnormal scans quit at higher rates (Tammemagi et al., 2014b). An analysis of MILD has shown that smoking cessation during the study is associated with a decrease in all-cause mortality (Pastorino et al., 2016). All lung cancer screening programs should incorporate proven smoking cessation strategies and work to improve the cessation rates.
Implementation of screening is complex. In the United States, CMS has linked screening reimbursement with an informed decision making session for the individual contemplating screening and has required submission of data from the screening program to a registry. The ACR already has approval for their registry system. Analysis of the registry data should facilitate programmatic improvement. As screening programs become more widespread in the United States and Canada further declines in lung cancer mortality, over those expected with smoking cessation alone, should occur similar to what has been seen with other successful screening programs such as cervical and colorectal cancer. Clearly, elimination of tobacco use by cessation and continued decreases in uptake will remain the best approaches for lowering the burden of tobacco related diseases long-term. Eventually it would be wonderful to see the need for lung cancer screening in ever smokers disappear. References Ali, M.U., Miller, J., et al., 2016. Screening for Lung Cancer: A Systematic Review and MetaAnalysis. Anon, 2016. Canadian task force on preventive health care guidelines, lung cancer. http:// canadiantaskforce.ca/ctfphc-guidelines/2015-lung-cancer/ (accessed May 17, 2016). Anon, d. American College of Radiology ACR-STR practice guideline for the performance and reporting of lung cancer screening thoracic computed tomographyhttp://www. acr.org/~/media/ACR/Documents/PGTS/guidelines/LungScreening.pdf (accessed February 22, 2015). Centers for Medicare and Medicaid Services, d. Decision memo for screening for lung cancer with low dose computed tomography (LDCT) (CAG-00439N)http://www.cms. gov/medicare-coverage-database/details/nca-decision-memo.aspx?NCAId=274 (accessed February 22, 2015). De Koning, H.J., Meza, R., Plevritis, S.K., et al., 2014. 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. 160, 311–320. Jemal, A., Center, M.M., DeSantis, C., Ward, E.M., 2010. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol. Biomark. Prev. 19 (8), 1893–1907 (Aug). Katki, H.A., Kovalchik, S.A., Berg, C.D., Cheung, L.C., Chaturvedi, A.C., 2016. Development and validation of risk models to select ever-smokers for CT lung cancer screening. JAMA http://dx.doi.org/10.1001/jama.2016.6255. Kovalchik, S.A., Tammemagi, M., Berg, C.D., et al., 2013. Targeting of low-dose CT screening according to the risk of lung-cancer death. N. Engl. J. Med. 369, 245–254. Manos, D., Seely, J.M., Taylor, J., et al., 2014. The lung reporting and data system (LURADS): a proposal for computed tomography screening. Can. Assoc. Radiol. J. 65 (2), 121–134. http://dx.doi.org/10.1016/j.carj.2014.03.004 (May). Marshall, H.M., Bowman, R.V., Yang, I.A., et al., 2013. Screening for lung cancer with lowdose computed tomography: a review of current status. J. Thorac. Dis. 5 (S5), S524–S539. Moyer, V.A., 2014. Screening for lung cancer: U.S. preventive services task force recommendation statement. Ann. Intern. Med. 160, 330–338. Oken, M.M., Hocking, W.G., Kvale, P.A., et al., 2011. Screening by chest radiograph and lung cancer mortality: the prostate, lung, colorectal, and ovarian (PLCO) randomized trial. JAMA 306, 1865–1873. Pastorino, U., Boffi, R., Marchiano, A., et al., 2016. Stopping smoking reduces mortality in low-dose computed tomography screening participants. J. Thorac. Oncol. 11, 693–699. Patz Jr., E.F., Greco, E., Gatsonis, C., et al., 2016. 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. (Mar 18. pii: S1470–2045(15)00,621-X). Pinsky, P.F., Gierada, D.S., Black, W., et al., 2015. Performance of lung-RADS in the National Lung Screening Trial. Ann. Intern. Med. 162, 485–491. Tammemagi, M.C., Berg, C.D., Riley, T.L., et al., 2014b. Impact of lung cancer screening results on smoking cessation. J. Natl. Cancer Inst. 106, dju084. Tammemagi, M.C., Church, T.R., Hocking, W.G., et al., 2014a. 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. 11, e10001764. Tammemägi, M.C., Katki, H.A., Hocking, W.G., Church, T.R., Caporaso, N., Kvale, P.A., Chaturvedi, A.K., Silvestri, G.A., Riley, T.L., Commins, J., Berg, C.D., 2013. Selection criteria for lung-cancer screening. N. Engl. J. Med. 368, 728–736. The National Lung Screening Trial Research Team, 2011. Reduced lung-cancer mortality with low-dose computed tomographic screening. N. Engl. J. Med. 365, 395–409.
Christine D. Berg Johns Hopkins Radiation Oncology and Molecular Radiation Sciences, Johns Hopkins School of Medicine, United States 31 May 2016 Available online xxxx
Please cite this article as: Berg, C.D., Lung cancer screening makes the GRADE, Prev. Med. (2016), http://dx.doi.org/10.1016/j.ypmed.2016.06.006
Contents lists available at ScienceDirect
Preventive Medicine journal homepage: www.elsevier.com/locate/ypmed
Editorial
Lung cancer screening makes the GRADE
Article: Screening for lung cancer: A systematic review and metaanalysis Authors: Ali M U, Miller J, Peirson L et al. Lung cancer mortality, when age-adjusted, is falling in Canada and the United States as a consequence of dissemination of effective antismoking efforts (Jemal et al., 2010). None-the-less it remains the leading cause of cancer death in males and females. Therapies, particularly targeted ones, are now making inroads in the dismal survival statistics. An important advance came with the definitive demonstration, now almost four years ago, in the National Lung Screening Trial (NLST) that three annual rounds of low-dose helical computerized tomography (LDCT) compared to chest-X-ray (CXR) lowered lung cancer mortality by 20.0% at 6.5 years (The National Lung Screening Trial Research Team, 2011). The Prostate, Lung, Colorectal and Ovarian Cancer Screening Trial (PLCO) results on CXR screening showed no benefit of CXR screening and lung cancer mortality results for CXR screening for a high-risk group in the PLCO that matched NLST criteria were comparable (Oken et al., 2011). As the NLST was the first randomized clinical trial (RCT) documenting a mortality reduction with screening for lung cancer, a public health challenge emerged. What recommendations for screening would be reasonable in the country or region in which it would be implemented? Specifically, which individuals at high-risk for lung cancer in which the benefits outweigh the harms would undergo screening and given the complexity how could this be achieved in the most cost-effective manner? In the United States, the United States Preventive Services Task Force (USPSTF) and the Centers for Medicare and Medicaid Services (CMS) recommended screening along the NLST criteria of ages 55–74, 30 pack years of smoking and if quit having quit within 15 years but extending the age to 80 and 77 respectively (Moyer, 2014; Centers for Medicare and Medicaid Services). In this issue, Ali and colleagues, from McMaster University and many with the McMaster Evidence Review and Synthesis Center evaluated the published literature on CXR, sputum cytology and LDCT screening for lung cancer to inform the Canadian Task Force on Preventive Health Care (CTFPHC) lung cancer screening guidelines (Ali et al., 2016). These guidelines have been released (Anon, 2016). The guidelines call for lung cancer screening in Canada to be in individuals who meet the NLST entry criteria. Currently, only three annual screens are recommended. The systematic review by Ali et al. includes literature published since the last review for the CTPHC which was performed in 2003. The only RCT results of helical CT screening published have been since then, as were the PLCO results. For the review of the quality of the evidence the Grading of Recommendations, Assessment, Development, and Evaluation (GRADE) system was applied. To my knowledge no other group
evaluating LDCT screening has applied this approach. It is a thorough approach that evaluates methodologic quality, statistical heterogeneity, directness of the body of evidence to the populations of interest, precision and reporting bias. Importantly it also considers the metric of whether or not further research would affect the estimate of effect. To date, only four studies of LDCT have been published, the NLST, Detection and Screening of Early Lung Cancer by Novel Imaging and Molecular Essays Trial (DANTE), Multi-centric Italian Lung Detection Trial (MILD) and Danish Lung Cancer Screening Trail (DLCST). (reviewed in Marshall, 2013) When evaluating DANTE, MILD and DLCST, Ali et al. correctly note that these trials are affected by very small sample size, entry criteria not focused on a consistently high risk group, variable screening intervals and in some cases short follow-up and were therefore rated as low quality. By contrast, the NLST has a large sample size, three rounds of annual screening and clear stopping rules to ensure that trial cessation and releasing of results occurred only when a statistically significant boundary was crossed. For full disclosure, I was the National Cancer Institute — United States Project Officer for the NLST. There remain several small trials, the United Kingdom Lung Cancer Screening Trial (UKLS), German Lung Cancer Screening Intervention Trial (LUSI) and ITALUNG and one moderately sized study Nederlands-Leuvens Longkanker Screenings Ondersoek Trial (NELSON) still to report (Marshall et al., 2013). The GRADE assessment by Ali et al. afforded the quality of the evidence from the NLST a “high” level meaning that it is very unlikely to have the evidence of effect overturned by additional research. In the interests of public health, Ali et al. rightly conclude that screening should be recommended. Many issues remain including which high risk groups to screen to maximize lives saved, definition and evaluation of positive screens to achieve high sensitivity with a specificity that limits false-positives and their attendant evaluation costs and harms from invasive procedures and frequency and duration of screening. Not all questions germane to lung cancer screening or many medical decisions for that matter, can be answered through clinical trials nor through innumerable reviews and meta-analyses of them. Ali et al. chose not to review any individualized risk assessment approaches or modeling. The Cancer Intervention and Surveillance Modeling Network (CISNET) modeling that informed the USPSTF recommendations employed micro-simulation natural history of lung cancer models (De Koning et al., 2014). Data from the NLST and PLCO were available to all of the modelers. Scenarios by grouped characteristics, age of starting, stopping, pack-years and quit duration and screening frequency, annual, biannual and triannual were assessed. A strategy similar to NLST entry criteria with age extending to 80 and continued annual screening beyond three years was judged to balance number of screens with lives saved. The recommendations by the CTFPHC extend only to three
http://dx.doi.org/10.1016/j.ypmed.2016.06.006 0091-7435/© 2016 Published by Elsevier Inc.
Please cite this article as: Berg, C.D., Lung cancer screening makes the GRADE, Prev. Med. (2016), http://dx.doi.org/10.1016/j.ypmed.2016.06.006
2
Editorial
annual rounds. It is unclear what is to occur then, as it is unlikely that over the next few years, screening programs will have been in existence long enough to generate adequate data about long term screening. Ali et al. did not address this issue. Other risk-based models have been developed utilizing individual level data and additional risk factors such as emphysema and family history, to estimate screening benefit based upon this individual risk. In two models one for lung cancer incidence and the other for lung cancer death, the lowest risk participants in the NLST benefited little or not all from screening (Tammemägi et al., 2013; Kovalchik et al., 2013). The lung cancer incidence model was applied to the PLCO showing that high risk individuals both within USPSTF and outside of USPSTF criteria would merit screening and that for the same numbers of individuals screened more lives would be saved by applying the incidence model for screening selection (Tammemagi et al., 2014a). A revised individual risk-based lung cancer death model was validated in the 1997–2001 National Health Interview Survey (NHIS) and then screening effect was projected in a more contemporary 2010–2012 NHIS dataset (Katki et al., 2016). This model was also more efficient than the USPSTF criteria. Those individuals at high risk outside the USPSTF criteria were preferentially African-American, current light smokers particularly women and heavy long-term smokers who had quit more than 15 years prior to risk assessment. Subsequent reviews and guideline development groups such as those that inform the USPSTF and the CTFPHC should look beyond randomized clinical trial data to encompass this information from risk-based models and also information that emerges from carefully conducted screening programs. Ali et al. used RCTs for harm assessment but also used quantitative designs. The harms of screening result primarily from evaluation of the positive examinations. In the NLST there was a high positive rate (24% per screen on average and 39% cumulative after three rounds) most of which (96%) were false-positives. Most follow-up was either clinical or imaging. Invasive testing to rule-out malignancy was also done. Ali et al. point out that death within 60 days of a positive examination was uncommon, only 1.5% in those undergoing invasive evaluation and 0.061% in all of those screened contrasting very favorably with the 6% decrease in all-cause mortality. Other quantitative data was similar. In the United States the American College of Radiology (ACR) has developed Lung-RADS and Manos E, et al., in Canada, LU-RADS to better classify screening LDCT results and aid in evaluation to lower the burden of positive screens (Anon; Manos et al., 2014). However, Pinsky et al. compared Lung-RADS to the NLST retrospectively and noted that while specificity was improved sensitivity suffered (Pinsky et al., 2015). It is unknown as to the clinical effect this will have and with further data emerging from screening programs modification of LungRADS and LU-RADS may be necessary. It is possible that a frequency other than annual screening may be reasonable for some individuals, particularly those with negative screens at baseline. Patz et al. retrospectively analyzed NLST data and showed that the risk of lung cancer was lower in those with a negative screen at baseline (Patz et al., 2016). If this can be confirmed in additional data sets, perhaps with demographic information that allows individualized risk assessment also, the personal and financial burden of screening may be reduced. Ali et al. reviewed two smoking cessation studies from NELSON and DLSCT. The NLST also has data of interest which they did not consider. Participants in the Lung Screening Study portion of the NLST were evaluated for smoking cessation and results analyzed by findings on LDCT and those with more abnormal scans quit at higher rates (Tammemagi et al., 2014b). An analysis of MILD has shown that smoking cessation during the study is associated with a decrease in all-cause mortality (Pastorino et al., 2016). All lung cancer screening programs should incorporate proven smoking cessation strategies and work to improve the cessation rates.
Implementation of screening is complex. In the United States, CMS has linked screening reimbursement with an informed decision making session for the individual contemplating screening and has required submission of data from the screening program to a registry. The ACR already has approval for their registry system. Analysis of the registry data should facilitate programmatic improvement. As screening programs become more widespread in the United States and Canada further declines in lung cancer mortality, over those expected with smoking cessation alone, should occur similar to what has been seen with other successful screening programs such as cervical and colorectal cancer. Clearly, elimination of tobacco use by cessation and continued decreases in uptake will remain the best approaches for lowering the burden of tobacco related diseases long-term. Eventually it would be wonderful to see the need for lung cancer screening in ever smokers disappear. References Ali, M.U., Miller, J., et al., 2016. Screening for Lung Cancer: A Systematic Review and MetaAnalysis. Anon, 2016. Canadian task force on preventive health care guidelines, lung cancer. http:// canadiantaskforce.ca/ctfphc-guidelines/2015-lung-cancer/ (accessed May 17, 2016). Anon, d. American College of Radiology ACR-STR practice guideline for the performance and reporting of lung cancer screening thoracic computed tomographyhttp://www. acr.org/~/media/ACR/Documents/PGTS/guidelines/LungScreening.pdf (accessed February 22, 2015). Centers for Medicare and Medicaid Services, d. Decision memo for screening for lung cancer with low dose computed tomography (LDCT) (CAG-00439N)http://www.cms. gov/medicare-coverage-database/details/nca-decision-memo.aspx?NCAId=274 (accessed February 22, 2015). De Koning, H.J., Meza, R., Plevritis, S.K., et al., 2014. 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. 160, 311–320. Jemal, A., Center, M.M., DeSantis, C., Ward, E.M., 2010. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol. Biomark. Prev. 19 (8), 1893–1907 (Aug). Katki, H.A., Kovalchik, S.A., Berg, C.D., Cheung, L.C., Chaturvedi, A.C., 2016. Development and validation of risk models to select ever-smokers for CT lung cancer screening. JAMA http://dx.doi.org/10.1001/jama.2016.6255. Kovalchik, S.A., Tammemagi, M., Berg, C.D., et al., 2013. Targeting of low-dose CT screening according to the risk of lung-cancer death. N. Engl. J. Med. 369, 245–254. Manos, D., Seely, J.M., Taylor, J., et al., 2014. The lung reporting and data system (LURADS): a proposal for computed tomography screening. Can. Assoc. Radiol. J. 65 (2), 121–134. http://dx.doi.org/10.1016/j.carj.2014.03.004 (May). Marshall, H.M., Bowman, R.V., Yang, I.A., et al., 2013. Screening for lung cancer with lowdose computed tomography: a review of current status. J. Thorac. Dis. 5 (S5), S524–S539. Moyer, V.A., 2014. Screening for lung cancer: U.S. preventive services task force recommendation statement. Ann. Intern. Med. 160, 330–338. Oken, M.M., Hocking, W.G., Kvale, P.A., et al., 2011. Screening by chest radiograph and lung cancer mortality: the prostate, lung, colorectal, and ovarian (PLCO) randomized trial. JAMA 306, 1865–1873. Pastorino, U., Boffi, R., Marchiano, A., et al., 2016. Stopping smoking reduces mortality in low-dose computed tomography screening participants. J. Thorac. Oncol. 11, 693–699. Patz Jr., E.F., Greco, E., Gatsonis, C., et al., 2016. 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. (Mar 18. pii: S1470–2045(15)00,621-X). Pinsky, P.F., Gierada, D.S., Black, W., et al., 2015. Performance of lung-RADS in the National Lung Screening Trial. Ann. Intern. Med. 162, 485–491. Tammemagi, M.C., Berg, C.D., Riley, T.L., et al., 2014b. Impact of lung cancer screening results on smoking cessation. J. Natl. Cancer Inst. 106, dju084. Tammemagi, M.C., Church, T.R., Hocking, W.G., et al., 2014a. 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. 11, e10001764. Tammemägi, M.C., Katki, H.A., Hocking, W.G., Church, T.R., Caporaso, N., Kvale, P.A., Chaturvedi, A.K., Silvestri, G.A., Riley, T.L., Commins, J., Berg, C.D., 2013. Selection criteria for lung-cancer screening. N. Engl. J. Med. 368, 728–736. The National Lung Screening Trial Research Team, 2011. Reduced lung-cancer mortality with low-dose computed tomographic screening. N. Engl. J. Med. 365, 395–409.
Christine D. Berg Johns Hopkins Radiation Oncology and Molecular Radiation Sciences, Johns Hopkins School of Medicine, United States 31 May 2016 Available online xxxx
Please cite this article as: Berg, C.D., Lung cancer screening makes the GRADE, Prev. Med. (2016), http://dx.doi.org/10.1016/j.ypmed.2016.06.006