European position statement on lung cancer screening

The Lancet Oncology

Volumn 18, Issue 12, 2017, Pages e754-e766

  Oudkerk, Matthijs ^a   Devaraj, Anand ^b   Vliegenthart, Rozemarijn ^a   Henzler, Thomas ^c   Prosch, Helmut ^d   Heussel, Claus P ^e,f,g   Bastarrika, Gorka ^h   Sverzellati, Nicola ⁱ   Mascalchi, Mario ^j   Delorme, Stefan ^k   Baldwin, David R ^l   Callister, Matthew E ^m   Becker, Nikolaus ^k   Heuvelmans, Marjolein A ^a   Rzyman, Witold ⁿ   Infante, Maurizio V ^o   Pastorino, Ugo ^p   Pedersen, Jesper H ^q   Paci, Eugenio ^r   Duffy, Stephen W ^s   de Koning, Harry ^t   Field, John K ^u   more..

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b ROYAL BROMPTON HOSPITAL   (United Kingdom)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

^e UNIVERSITY OF HEIDELBERG   (Germany)

^f German Center for Lung Research   (Germany)

^g UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^h UNIVERSITY CLINIC OF NAVARRA   (Spain)

ⁱ UNIVERSITY OF PARMA   (Italy)

^j UNIVERSITY OF FLORENCE   (Italy)

^k GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^l NOTTINGHAM UNIVERSITY HOSPITALS NHS TRUST   (United Kingdom)

^m ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

ⁿ MEDICAL UNIVERSITY OF GDANSK   (Poland)

^o UNIVERSITY HOSPITAL OF VERONA   (Italy)

^p NATIONAL CANCER INSTITUTE   (Italy)

^q UNIVERSITY OF COPENHAGEN   (Denmark)

^r CANCER RESEARCH AND PREVENTION INSTITUTE ISPO   (Italy)

^s QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^t ERASMUS MEDICAL CENTER   (Netherlands)

^u UNIVERSITY OF LIVERPOOL   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; MICRORNA;

BIOBANK; BIOLOGICAL MODEL; BREATH ANALYSIS; BRONCHOSCOPY; BRONCHUS; CANCER INCIDENCE; CANCER MORTALITY; CANCER RISK; CANCER SCREENING; CANCER SUSCEPTIBILITY; CHRONIC OBSTRUCTIVE LUNG DISEASE; CLINICAL COMPETENCE; CLINICAL PRACTICE; CLINICAL PROTOCOL; CONSENSUS DEVELOPMENT; CORONARY ARTERY CALCIFICATION; COST EFFECTIVENESS ANALYSIS; DIAGNOSTIC ACCURACY; DISTRESS SYNDROME; EARLY DIAGNOSIS; EMPHYSEMA; EUROPEAN UNION; EVIDENCE BASED MEDICINE; FALSE POSITIVE RESULT; GENE EXPRESSION; HARM REDUCTION; HEALTH CARE ACCESS; HEALTH CARE PLANNING; HEALTH HAZARD; HEALTH PROGRAM; HIGH RISK PATIENT; HUMAN; INCIDENT SCREENING ROUND; INCIDENTAL FINDING; INTERMETHOD COMPARISON; LOW ENERGY RADIATION; LUNG CANCER; LUNG NODULE; LUNG VOLUME; MASS SCREENING; MENTAL DISEASE; METHODOLOGY; OVERDIAGNOSIS; PATIENT INFORMATION; PATIENT REFERRAL; PATIENT SELECTION; PHYSICAL HARM; PRACTICE GUIDELINE; PREVALENCE; PRIORITY JOURNAL; PSYCHOLOGICAL HARM; QUALITY CONTROL; RADIATION DOSE; RADIATION EXPOSURE; RADIATION HAZARD; RADIOLOGICAL PARAMETERS; RADIOMIC ANALYSIS; REVIEW; RISK ASSESSMENT; RISK FACTOR; SENSITIVITY AND SPECIFICITY; SMOKING; SMOKING CESSATION; SOLID INCIDENT NODULE; STANDARD; TEAMWORK; THORAX RADIOGRAPHY; TUMOR VOLUME; VOLUME DOUBLING TIME; X-RAY COMPUTED TOMOGRAPHY; EARLY CANCER DIAGNOSIS; EUROPE; FEMALE; INCIDENCE; LUNG TUMOR; MALE; PROCEDURES; STANDARDS;

EARLY DETECTION OF CANCER; EUROPE; FEMALE; HUMANS; INCIDENCE; LUNG NEOPLASMS; MALE; MASS SCREENING; PRACTICE GUIDELINES AS TOPIC; TOMOGRAPHY, X-RAY COMPUTED;

EID: 85035357095     PISSN: 14702045     EISSN: 14745488     Source Type: Journal    
DOI: 10.1016/S1470-2045(17)30861-6     Document Type: Review

References (91)

1. National Lung Screening Trial Research Team, Aberle, DR, Adams, AM, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med 365 (2011), 395–409.
2. van Klaveren, RJ, Oudkerk, M, Prokop, M, et al. Management of lung nodules detected by volume CT scanning. N Engl J Med 361 (2009), 2221–2229.
3. Sverzellati, N, Silva, M, Calareso, G, et al. Low-dose computed tomography for lung cancer screening: comparison of performance between annual and biennial screen. Eur Radiol 26 (2016), 3821–3829.
4. Paci, E, Puliti, D, Lopes Pegna, A, et al. Mortality, survival and incidence rates in the ITALUNG randomised lung cancer screening trial. Thorax 72 (2017), 825–831.
5. Infante, M, Cavuto, S, Lutman, FR, et al. 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 191 (2015), 1166–1175.
6. Wille, MM, Dirksen, A, Ashraf, H, et al. Results of the randomized danish lung cancer screening trial with focus on high-risk profiling. Am J Respir Crit Care Med 193 (2016), 542–551.
7. Becker, N, Motsch, E, Gross, ML, et al. Randomized study on early detection of lung cancer with MSCT in Germany: results of the first 3 years of follow-up after randomization. J Thorac Oncol 10 (2015), 890–896.
8. Field, JK, Duffy, SW, Baldwin, DR, et al. 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 20 (2016), 1–146.
9. Field, JK, van Klaveren, R, Pedersen, JH, et al. European randomized lung cancer screening trials: Post NLST. J Surg Oncol 108 (2013), 280–286.
10. Van den Bergh, KA, Essink-Bot, ML, Bunge, EM, et al. Impact of computed tomography screening for lung cancer on participants in a randomized controlled trial (NELSON trial). Cancer 113 (2008), 396–404.
11. Van den Bergh, KA, Essink-Bot, ML, Borsboom, GJ, et al. Short-term health-related quality of life consequences in a lung cancer CT screening trial (NELSON). Br J Cancer 102 (2010), 27–34.
12. Fontana, RS, Sanderson, DR, Woolner, LB, Taylor, WF, Miller, WE, Muhm, JR, Lung cancer screening: the Mayo program. J Occup Med 28 (1986), 746–750.
13. Oken, MM, Hocking, WG, Kvale, PA, et al. Screening by chest radiograph and lung cancer mortality: the prostate, lung, colorectal, and ovarian (PLCO) randomized trial. JAMA 306 (2011), 1865–1873.
14. Henschke, CI, McCauley, DI, Yankelevitz, DF, et al. Early lung cancer action project: overall design and findings from baseline screening. Lancet 354 (1999), 99–105.
15. Biederer, J, Ohno, Y, Hatabu, H, et al. Screening for lung cancer: does MRI have a role?. Eur J Radiol 86 (2017), 353–360.
16. Horeweg, N, van der Aalst, CM, Vliegenthart, R, et al. Volumetric computed tomography screening for lung cancer: three rounds of the NELSON trial. Eur Respir J 42 (2013), 1659–1667.
17. Walter, JE, Heuvelmans, MA, de Jong, PA, et al. 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 17 (2016), 907–916.
18. Marcus, PM, Bergstralh, EJ, Fagerstrom, RM, et al. Lung cancer mortality in the Mayo Lung Project: impact of extended follow-up. J Natl Cancer Inst 92 (2000), 1308–1316.
19. Tammemagi, MC, Schmidt, H, Martel, S, et al. Participant selection for lung cancer screening by risk modelling (the Pan-Canadian Early Detection of Lung Cancer [PanCan] study): a single-arm, prospective study. Lancet Oncol 18 (2017), 1523–1531.
20. Veronesi, G, Bellomi, M, Mulshine, JL, et al. Lung cancer screening with low-dose computed tomography: a non-invasive diagnostic protocol for baseline lung nodules. Lung Cancer 61 (2008), 340–349.
21. Horeweg, N, van Rosmalen, J, Heuvelmans, MA, et al. 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 15 (2014), 1332–1341.
22. Field, JK, Oudkerk, M, Pedersen, JH, Duffy, SW, Prospects for population screening and diagnosis of lung cancer. Lancet 382 (2013), 732–741.
23. Infante, M, Sestini, S, Galeone, C, et al. Lung cancer screening with low-dose spiral computed tomography: evidence from a pooled analysis of two Italian randomized trials. Eur J Cancer Prev 26 (2016), 324–329.
24. Cressman, S, Peacock, SJ, Tammemagi, MC, et al. The cost-effectiveness of high-risk lung cancer screening and drivers of program efficiency. J Thorac Oncol 12 (2017), 1210–1222.
25. Gonzalez, J, Marin, M, Sanchez-Salcedo, P, Zulueta, JJ, Lung cancer screening in patients with chronic obstructive pulmonary disease. Ann Transl Med, 4, 2016, 160.
26. Murray, CJ, Vos, T, Lozano, R, et al. Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380 (2012), 2197–2223.
27. Cassidy, A, Myles, JP, van Tongeren, M, et al. The LLP risk model: an individual risk prediction model for lung cancer. Br J Cancer 98 (2008), 270–276.
28. Bach, PB, Kattan, MW, Thornquist, MD, et al. Variations in lung cancer risk among smokers. J Natl Cancer Inst 95 (2003), 470–478.
29. Spitz, MR, Hong, WK, Amos, CI, et al. A risk model for prediction of lung cancer. J Natl Cancer Inst 99 (2007), 715–726.
30. Tammemagi, MC, Katki, HA, Hocking, WG, et al. Selection criteria for lung-cancer screening. N Engl J Med 368 (2013), 728–736.
31. Kovalchik, SA, Tammemagi, M, Berg, CD, et al. Targeting of low-dose CT screening according to the risk of lung-cancer death. N Engl J Med 369 (2013), 245–254.
32. Katki, HA, Kovalchik, SA, Berg, CD, Cheung, LC, Chaturvedi, AK, Development and validation of risk models to select ever-smokers for CT lung cancer screening. JAMA 315 (2016), 2300–2311.
33. Raji, OY, Duffy, SW, Agbaje, OF, et al. Predictive accuracy of the Liverpool Lung Project risk model for stratifying patients for computed tomography screening for lung cancer: a case-control and cohort validation study. Ann Intern Med 157 (2012), 242–250.
34. Field JK, Gaynor ES, Duffy SW, et al. Liverpool healthy lung project: a primary care initiative to identify hard to reach individuals with a high risk of developing lung cancer. AACR Annual Meeting; Washington, DC, USA; April 1–5, 2017. 4220.
35. Field, JK, Marcus, M, Maroni, R, et al. Liverpool Healthy Lung project. http://www.liverpoolccg.nhs.uk/health-and-services/healthy-lungs/, 2017 (accessed June 9, 2017).
36. Li, K, Husing, A, Sookthai, D, et al. 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) 8 (2015), 777–785.
37. Ten Haaf, K, Jeon, J, Tammemagi, MC, et al. Risk prediction models for selection of lung cancer screening candidates: A retrospective validation study. PLoS Med, 14, 2017, e1002277.
38. Weber, M, Yap, S, Goldsbury, D, et al. Identifying high risk individuals for targeted lung cancer screening: Independent validation of the PLCOm2012 risk prediction tool. Int J Cancer 141 (2017), 242–253.
39. Hung, RJ, McKay, JD, Gaborieau, V, et al. A susceptibility locus for lung cancer maps to nicotinic acetylcholine receptor subunit genes on 15q25. Nature 452 (2008), 633–637.
40. Amos, CI, Dennis, J, Wang, Z, et al. The OncoArray consortium: a network for understanding the genetic architecture of common cancers. Cancer Epidemiol Biomarkers Prev 26 (2017), 126–135.
41. Sestini, S, Boeri, M, Marchiano, A, et al. Circulating microRNA signature as liquid-biopsy to monitor lung cancer in low-dose computed tomography screening. Oncotarget 6 (2015), 32868–32877.
42. Silvestri, GA, Vachani, A, Whitney, D, et al. A bronchial genomic classifier for the diagnostic evaluation of lung cancer. N Engl J Med 373 (2015), 243–251.
43. Broza, YY, Kremer, R, Tisch, U, et al. A nanomaterial-based breath test for short-term follow-up after lung tumor resection. Nanomedicine 9 (2013), 15–21.
44. Owlstone Medical. LuCID: a multi-centre prospective trial for lung cancer screening. https://www.owlstonemedical.com/clinical-pipeline/lucid/, 2016 (accessed July 1, 2017).
45. Postmus, PE, Kerr, KM, Oudkerk, M, et al. Early and locally advanced non-small-cell lung cancer (NSCLC): ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 28:suppl 4 (2017), iv1–iv21.
46. Pedersen, JH, Rzyman, W, Veronesi, G, et al. Recommendations from the European Society of Thoracic Surgeons (ESTS) regarding computed tomography screening for lung cancer in Europe. Eur J Cardiothorac Surg 51 (2017), 411–420.
47. Rampinelli, C, De Marco, P, Origgi, D, et al. Exposure to low dose computed tomography for lung cancer screening and risk of cancer: secondary analysis of trial data and risk-benefit analysis. BMJ, 356, 2017, j347.
48. Tammemagi, MC, Berg, CD, Riley, TL, Cunningham, CR, Taylor, KL, Impact of lung cancer screening results on smoking cessation. J Natl Cancer Inst, 106, 2014, dju084.
49. Ashraf, H, Tonnesen, P, Holst Pedersen, J, Dirksen, A, Thorsen, H, Dossing, M, Effect of CT screening on smoking habits at 1-year follow-up in the Danish Lung Cancer Screening Trial (DLCST). Thorax 64 (2009), 388–392.
50. Brain, K, Carter, B, Lifford, KJ, et al. Impact of low-dose CT screening on smoking cessation among high-risk participants in the UK Lung Cancer Screening Trial. Thorax 72 (2017), 912–918.
51. Fintelmann, FJ, Bernheim, A, Digumarthy, SR, et al. The 10 pillars of lung cancer screening: rationale and logistics of a lung cancer screening program. Radiographics 35 (2015), 1893–1908.
52. 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 13:suppl 2 (2016), R25–R29.
53. Pinsky, PF, Gierada, DS, Black, W, et al. Performance of lung-RADS in the National Lung Screening Trial: a retrospective assessment. Ann Intern Med 162 (2015), 485–491.
54. Mehta, HJ, Mohammed, TL, Jantz, MA, The American College of Radiology lung imaging reporting and data system: potential drawbacks and need for revision. Chest 151 (2017), 539–543.
55. Li, K, Yip, R, Avila, R, Henschke, CI, Yankelevitz, DF, Size and growth assessment of pulmonary nodules: consequences of the rounding. J Thorac Oncol 12 (2016), 657–662.
56. McWilliams, A, Tammemagi, MC, Mayo, JR, et al. Probability of cancer in pulmonary nodules detected on first screening CT. N Engl J Med 369 (2013), 910–919.
57. van Riel, SJ, Ciompi, F, Jacobs, C, et al. Malignancy risk estimation of screen-detected nodules at baseline CT: comparison of the PanCan model, Lung-RADS and NCCN guidelines. Eur Radiol 27 (2017), 4019–4029.
58. Heuvelmans, MA, Walter, JE, Vliegenthart, R, et al. Disagreement of diameter and volume measurements for pulmonary nodule size estimation in CT lung cancer screening. Thorax, 2017 published online Oct 22. DOI: 10.1136/thoraxjnl-2017-210770.
59. Heuvelmans M, Vliegenthart R, van Ooijen P. Nodule size is poorly represented by nodule diameter in low–dose CT lung cancer screening. IASLC 17th world conference on lung cancer; Vienna, Austria; Dec 4–7, 2016. P1.03–042.
60. Public Health England. Breast screening: programme consolidated standards. 2017, Public Health England, London.
61. Perry, N, Broeders, M, de Wolf, C, Tornberg, S, Holland, R, von Karsa, L, European guidelines for quality assurance in breast cancer screening and diagnosis. Fourth edition—summary document. Ann Oncol 19 (2008), 614–622.
62. LCRB Dutch breast cancer—focus on early disease. http://www.lrcb.nl/en/breast-cancer/audit/, 2017 (accessed May 15, 2017).
63. CT Volumetry Technical Committee. Lung nodule assessment in CT screening profile. 2017. QIBA. http://qibawiki.rsna.org/images/f/fb/QIBA_CT_Vol_LungNoduleAssessmentInCTScreening_2017.07.rev15.pdf (accessed Aug 01, 2017).
64. Heuvelmans, MA, Vliegenthart, R, de Koning, HJ, et al. Quantification of growth patterns of screen-detected lung cancers: the NELSON study. Lung Cancer 108 (2017), 48–54.
65. de Hoop, B, Gietema, H, van Ginneken, B, Zanen, P, Groenewegen, G, Prokop, M, A comparison of six software packages for evaluation of solid lung nodules using semi-automated volumetry: what is the minimum increase in size to detect growth in repeated CT examinations. Eur Radiol 19 (2009), 800–808.
66. Scholten, ET, de Jong, PA, Jacobs, C, et al. Interscan variation of semi-automated volumetry of subsolid pulmonary nodules. Eur Radiol 25 (2015), 1040–1047.
67. Chung, K, Jacobs, C, Scholten, ET, et al. Lung-RADS category 4X: does it improve prediction of malignancy in subsolid nodules?. Radiology 284 (2017), 264–271.
68. Midthun, DE, Jett, JR, Screening for lung cancer: the US studies. J Surg Oncol 108 (2013), 275–279.
69. Bach, PB, Mirkin, JN, Oliver, TK, et al. Benefits and harms of CT screening for lung cancer: a systematic review. JAMA 307 (2012), 2418–2429.
70. Callister, ME, Baldwin, DR, Akram, AR, et al. British Thoracic Society guidelines for the investigation and management of pulmonary nodules. Thorax 70:suppl 2 (2015), ii1–ii54.
71. Henschke, CI, Naidich, DP, Yankelevitz, DF, et al. Early lung cancer action project: initial findings on repeat screenings. Cancer 92 (2001), 153–159.
72. Henschke, CI, Yankelevitz, DF, Libby, DM, Pasmantier, MW, Smith, JP, Miettinen, OS, Survival of patients with stage I lung cancer detected on CT screening. N Engl J Med 355 (2006), 1763–1771.
73. Wilson, DO, Weissfeld, JL, Fuhrman, CR, et al. The Pittsburgh Lung Screening Study (PLuSS): outcomes within 3 years of a first computed tomography scan. Am J Respir Crit Care Med 178 (2008), 956–961.
74. Swensen, SJ, Jett, JR, Sloan, JA, et al. Screening for lung cancer with low-dose spiral computed tomography. Am J Respir Crit Care Med 165 (2002), 508–513.
75. Henschke, CI, Yankelevitz, DF, Yip, R, et al. Lung cancers diagnosed at annual CT screening: volume doubling times. Radiology 263 (2012), 578–583.
76. Carter, D, Vazquez, M, Flieder, DB, et al. Comparison of pathologic findings of baseline and annual repeat cancers diagnosed on CT screening. Lung Cancer 56 (2007), 193–199.
77. Xu, DM, Yip, R, Smith, JP, Yankelevitz, DF, Henschke, CI, Investigators, IE, Retrospective review of lung cancers diagnosed in annual rounds of CT screening. AJR Am J Roentgenol 203 (2014), 965–972.
78. Cancer Research UK. Pulmonary nodule risk. https://itunes.apple.com/gb/app/pulmonary-nodule-risk/id1142255949?mt=8, 2017 (accessed May 15, 2017).
79. Herder, GJ, van Tinteren, H, Golding, RP, et al. Clinical prediction model to characterize pulmonary nodules: validation and added value of 18F-fluorodeoxyglucose positron emission tomography. Chest 128 (2005), 2490–2496.
80. US Preventive Services Task Force. Final Update Summary: Lung Cancer: Screening. http://www.uspreventiveservicestaskforce.org/Page/Document/UpdateSummaryFinal/lung-cancer-screening, 2015 (accessed July 26, 2017).
81. Yousaf-Khan, U, van der Aalst, C, de Jong, PA, et al. Final screening round of the NELSON lung cancer screening trial: the effect of a 2.5-year screening interval. Thorax 72 (2017), 48–56.
82. Ten Haaf, K, Tammemagi, MC, Bondy, SJ, et al. Performance and cost-effectiveness of computed tomography lung cancer screening scenarios in a population-based setting: a microsimulation modeling analysis in Ontario, Canada. PLoS Med, 14, 2017, e1002225.
83. Pastorino, U, Rossi, M, Rosato, V, et al. Annual or biennial CT screening versus observation in heavy smokers: 5-year results of the MILD trial. Eur J Cancer Prev 21 (2012), 308–315.
84. Duffy, SW, Field, JK, Allgood, PC, Seigneurin, A, Translation of research results to simple estimates of the likely effect of a lung cancer screening programme in the United Kingdom. Br J Cancer 110 (2014), 1834–1840.
85. Yankelevitz, D, Henschke, C, Lung cancer: low-dose CT screening—determining the right interval. Nat Rev Clin Oncol 13 (2016), 533–534.
86. Yousaf-Khan, U, van der Aalst, C, de Jong, PA, et al. Risk stratification based on screening history: the NELSON lung cancer screening study. Thorax 72 (2017), 819–824.
87. Patz, EF Jr, Greco, E, Gatsonis, C, Pinsky, P, Kramer, BS, Aberle, DR, 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 17 (2016), 590–599.
88. Dunn, CE, Edwards, A, Carter, B, Field, JK, Brain, K, Lifford, KJ, The role of screening expectations in modifying short-term psychological responses to low-dose computed tomography lung cancer screening among high-risk individuals. Patient Educ Couns 100 (2017), 1572–1579.
89. Field, JK, Duffy, SW, Devaraj, A, Baldwin, DR, Implementation planning for lung cancer screening: five major challenges. Lancet Respir Med 4 (2016), 685–687.
90. Ciompi, F, Chung, K, van Riel, SJ, et al. Towards automatic pulmonary nodule management in lung cancer screening with deep learning. Sci Rep, 7, 2017, 46479.
91. Field, JK, Perspective: the screening imperative. Nature, 513, 2014, S7.