Interpretation of the NCCN clinical practice guidelines in oncology for lung cancer screening (version 2.2023)_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

LUO Guoqing , WANG Wenjie , LU Xiao ,  LI Ning ,  GENG Qing

Department of Thoracic Surgery, Renmin Hospital of Wuhan University, Wuhan, 430060, P. R. China;

Corresponding author：

LI Ning, Email: md.lining@whu.edu.cn; GENG Qing, Email: gengqingwhu@whu.edu.cn

Keywords：

Lung cancer screening; NCCN guideline; guideline interpretation

DOI：

10.7507/1007-4848.202306011

Video：

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Lung cancer is the malignant tumor with the highest incidence rate in men and the highest mortality rate in men and women in China, and the incidence and mortality rates are still increasing. Lung cancer screening is an important initiative for early detection of lung cancer and improvement of prognosis. The National Comprehensive Cancer Network (NCCN) updates the NCCN Clinical Practice Guidelines for Lung Cancer Screening annually, and the 2023 V2 edition was released in May 2023. The guidelines are based on the latest research advances and high-level evidence-based medical evidence to establish screening criteria for lung cancer, especially for non-small cell lung cancer, which is the most common and highly regarded type of lung cancer, and has received widespread attention from physicians worldwide. In this article, the latest version of the guideline will be interpreted based on China's national situation and Chinese lung cancer screening guidelines, with the aim of providing an updated reference for lung cancer screening in China.

Citation： LUO Guoqing, WANG Wenjie, LU Xiao, LI Ning, GENG Qing. Interpretation of the NCCN clinical practice guidelines in oncology for lung cancer screening (version 2.2023). Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2023, 30(9): 1217-1223. doi: 10.7507/1007-4848.202306011 Copy

1.	Siegel RL, Miller KD, Fuchs HE, et al. Cancer statistics, 2022. CA Cancer J Clin, 2022, 72(1): 7-33.
2.	Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
3.	尹周一, 王梦圆, 游伟程, 等. 2022美国癌症统计报告解读及中美癌症流行情况对比. 肿瘤综合治疗电子杂志, 2022, 8(2): 54-63.
4.	Zeng H, Chen W, Zheng R, et al. Changing cancer survival in China during 2003-15: A pooled analysis of 17 population-based cancer registries. Lancet Glob Health, 2018, 6(5): e555-e567.
5.	Allemani C, Matsuda T, Di Carlo V, et al. Global surveillance of trends in cancer survival 2000-14 (CONCORD-3): Analysis of individual records for 37513025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet, 2018, 391(10125): 1023-1075.
6.	Zeng H, Ran X, An L, et al. Disparities in stage at diagnosis for five common cancers in China: A multicentre, hospital-based, observational study. Lancet Public Health, 2021, 6(12): e877-e887.
7.	Travis WD, Brambilla E, Noguchi M, et al. International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol, 2011, 6(2): 244-285.
8.	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, 2016, 193(5): 542-551.
9.	Miller DL, Mayfield WR, Luu TD, et al. Community-based multidisciplinary computed tomography screening program improves lung cancer survival. Ann Thorac Surg, 2016, 101(5): 1864-1869.
10.	Horeweg N, van der Aalst CM, Thunnissen E, et al. Characteristics of lung cancers detected by computer tomography screening in the randomized NELSON trial. Am J Respir Crit Care Med, 2013, 187(8): 848-854.
11.	Becker N, Motsch E, Trotter A, et al. Lung cancer mortality reduction by LDCT screening: Results from the randomized German LUSI trial. Int J Cancer, 2020, 146(6): 1503-1513.
12.	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, 2016, 17(7): 907-916.
13.	Aberle DR, Adams AM, Berg CD, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med, 2011, 365(5): 395-409.
14.	Aberle DR, DeMello S, Berg CD, et al. Results of the two incidence screenings in the National Lung Screening Trial. N Engl J Med, 2013, 369(10): 920-931.
15.	范亚光, 周清华, 乔友林, 等. 中国肺癌低剂量CT筛查指南(2023年版). 中国肺癌杂志, 2023, 26(1): 1-9.
16.	赫捷, 李霓, 陈万青, 等. 中国肺癌筛查与早诊早治指南(2021, 北京). 中国肿瘤, 2021, 30(2): 81-111.
17.	Vachani A, Carroll NM, Simoff MJ, et al. Stage migration and lung cancer incidence after initiation of low-dose computed tomography screening. J Thorac Oncol, 2022, 17(12): 1355-1364.
18.	National Comprehensive Cancer Network. NCCN clinical practice guidelines in oncology: Lung cancer screening (version 2.2023). URL: htps:/www.nccn.org.
19.	Sands J, Tammemägi MC, Couraud S, et al. Lung screening benefits and challenges: A review of the data and outline for implementation. J Thorac Oncol, 2021, 16(1): 37-53.
20.	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, 2017, 18(11): 1523-1531.
21.	Jha P, Peto R. Global effects of smoking, of quitting, and of taxing tobacco. N Engl J Med, 2014, 370(1): 60-68.
22.	Office of the Surgeon General (US), Office on Smoking and Health (US). The Health Consequences of Smoking: A Report of the Surgeon General. Atlanta (GA): Centers for Disease Control and Prevention (US), 2004.
23.	Darby S, Hill D, Auvinen A, et al. Radon in homes and risk of lung cancer: Collaborative analysis of individual data from 13 European case-control studies. BMJ, 2005, 330(7485): 223.
24.	Driscoll T, Nelson DI, Steenland K, et al. The global burden of disease due to occupational carcinogens. Am J Ind Med, 2005, 48(6): 419-431.
25.	Loomis D, Guha N, Hall AL, et al. Identifying occupational carcinogens: An update from the IARC Monographs. Occup Environ Med, 2018, 75(8): 593-603.
26.	Delva F, Margery J, Laurent F, et al. Medical follow-up of workers exposed to lung carcinogens: French evidence-based and pragmatic recommendations. BMC Public Health, 2017, 17(1): 191.
27.	O'Dwyer E, Halpenny DF and Ginsberg MS. Lung cancer screening in patients with previous malignancy: Is this cohort at increased risk for malignancy? Eur Radiol, 2021, 31(1): 458-467.
28.	Wu GX, Nelson RA, Kim JY, et al. Non-small cell lung cancer as a second primary among patients with previous malignancy: Who is at risk? Clin Lung Cancer, 2017, 18(5): 543-550.
29.	Yang IA, Holloway JW, Fong KM. Genetic susceptibility to lung cancer and co-morbidities. J Thorac Dis, 2013, 5 (Suppl 5): S454-S462.
30.	Hubbard R, Venn A, Lewis S, et al. Lung cancer and cryptogenic fibrosing alveolitis. A population-based cohort study. Am J Respir Crit Care Med, 2000, 161(1): 5-8.
31.	Coté ML, Liu M, Bonassi S, et al. Increased risk of lung cancer in individuals with a family history of the disease: A pooled analysis from the International Lung Cancer Consortium. Eur J Cancer, 2012, 48(13): 1957-1968.
32.	Tammemägi MC, Katki HA, Hocking WG, et al. Selection criteria for lung-cancer screening. N Engl J Med, 2013, 368(8): 728-736.
33.	Tammemägi MC, Church TR, Hocking WG, et al. Evaluation of the lung cancer risks at which to screen ever- and never-smokers: Screening rules applied to the PLCO and NLST cohorts. PLoS Med, 2014, 11(12): e1001764.
34.	Pasquinelli MM, Tammemägi MC, Kovitz KL, et al. Risk prediction model versus united states preventive services task force lung cancer screening eligibility criteria: Reducing race disparities. J Thorac Oncol, 2020, 15(11): 1738-1747.
35.	Tammemägi MC, Ten Haaf K, Toumazis I, et al. Development and validation of a multivariable lung cancer risk prediction model that includes low-dose computed tomography screening results: A secondary analysis of data from the National Lung Screening Trial. JAMA Netw Open, 2019, 2(3): e190204.
36.	McWilliams A, Tammemagi MC, Mayo JR, et al. Probability of cancer in pulmonary nodules detected on first screening CT. N Engl J Med, 2013, 369(10): 910-919.
37.	Yang D, Liu Y, Bai C, et al. Epidemiology of lung cancer and lung cancer screening programs in China and the United States. Cancer Lett, 2020, 468: 82-87.
38.	Marshall HM, Bowman RV, Yang IA, et al. Screening for lung cancer with low-dose computed tomography: A review of current status. J Thorac Dis, 2013, 5 (Suppl 5): S524-S539.
39.	Christenson SA, Smith BM, Bafadhel M, et al. Chronic obstructive pulmonary disease. Lancet, 2022, 399(10342): 2227-2242.
40.	Gould MK, Donington J, Lynch WR, et al. Evaluation of individuals with pulmonary nodules: When is it lung cancer? Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest, 2013, 143(5 Suppl): e93S-e120S.
41.	Kazerooni EA, Armstrong MR, Amorosa JK, et al. ACR CT accreditation program and the lung cancer screening program designation. J Am Coll Radiol, 2016, 13(2 Suppl): R30-R34.
42.	Gardiner N, Jogai S, Wallis A. The revised lung adenocarcinoma classification: An imaging guide. J Thorac Dis, 2014, 6(Suppl 5): S537-S546.
43.	Naidich DP, Bankier AA, MacMahon H, et al. Recommendations for the management of subsolid pulmonary nodules detected at CT: A statement from the Fleischner Society. Radiology, 2013, 266(1): 304-317.
44.	Patz EF Jr , Greco E, Gatsonis C, et al. Lung cancer incidence and mortality in National Lung Screening Trial participants who underwent low-dose CT prevalence screening: A retrospective cohort analysis of a randomised, multicentre, diagnostic screening trial. Lancet Oncol, 2016, 17(5): 590-599.
45.	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, 2017, 72(9): 819-824.
46.	Detterbeck FC, Bolejack V, Arenberg DA, et al. The IASLC Lung Cancer Staging Project: Background data and proposals for the classification of lung cancer with separate tumor nodules in the forthcoming eighth edition of the TNM classification for lung cancer. J Thorac Oncol, 2016, 11(5): 681-692.
47.	de Koning HJ, van der Aalst CM, de Jong PA, et al. Reduced lung-cancer mortality with volume CT screening in a randomized trial. N Engl J Med, 2020, 382(6): 503-513.
48.	Pastorino U, Silva M, Sestini S, et al. Prolonged lung cancer screening reduced 10-year mortality in the MILD trial: New confirmation of lung cancer screening efficacy. Ann Oncol, 2019, 30(7): 1162-1169.

1. Siegel RL, Miller KD, Fuchs HE, et al. Cancer statistics, 2022. CA Cancer J Clin, 2022, 72(1): 7-33.
2. Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
3. 尹周一, 王梦圆, 游伟程, 等. 2022美国癌症统计报告解读及中美癌症流行情况对比. 肿瘤综合治疗电子杂志, 2022, 8(2): 54-63.
4. Zeng H, Chen W, Zheng R, et al. Changing cancer survival in China during 2003-15: A pooled analysis of 17 population-based cancer registries. Lancet Glob Health, 2018, 6(5): e555-e567.
5. Allemani C, Matsuda T, Di Carlo V, et al. Global surveillance of trends in cancer survival 2000-14 (CONCORD-3): Analysis of individual records for 37513025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet, 2018, 391(10125): 1023-1075.
6. Zeng H, Ran X, An L, et al. Disparities in stage at diagnosis for five common cancers in China: A multicentre, hospital-based, observational study. Lancet Public Health, 2021, 6(12): e877-e887.
7. Travis WD, Brambilla E, Noguchi M, et al. International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol, 2011, 6(2): 244-285.
8. 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, 2016, 193(5): 542-551.
9. Miller DL, Mayfield WR, Luu TD, et al. Community-based multidisciplinary computed tomography screening program improves lung cancer survival. Ann Thorac Surg, 2016, 101(5): 1864-1869.
10. Horeweg N, van der Aalst CM, Thunnissen E, et al. Characteristics of lung cancers detected by computer tomography screening in the randomized NELSON trial. Am J Respir Crit Care Med, 2013, 187(8): 848-854.
11. Becker N, Motsch E, Trotter A, et al. Lung cancer mortality reduction by LDCT screening: Results from the randomized German LUSI trial. Int J Cancer, 2020, 146(6): 1503-1513.
12. 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, 2016, 17(7): 907-916.
13. Aberle DR, Adams AM, Berg CD, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med, 2011, 365(5): 395-409.
14. Aberle DR, DeMello S, Berg CD, et al. Results of the two incidence screenings in the National Lung Screening Trial. N Engl J Med, 2013, 369(10): 920-931.
15. 范亚光, 周清华, 乔友林, 等. 中国肺癌低剂量CT筛查指南(2023年版). 中国肺癌杂志, 2023, 26(1): 1-9.
16. 赫捷, 李霓, 陈万青, 等. 中国肺癌筛查与早诊早治指南(2021, 北京). 中国肿瘤, 2021, 30(2): 81-111.
17. Vachani A, Carroll NM, Simoff MJ, et al. Stage migration and lung cancer incidence after initiation of low-dose computed tomography screening. J Thorac Oncol, 2022, 17(12): 1355-1364.
18. National Comprehensive Cancer Network. NCCN clinical practice guidelines in oncology: Lung cancer screening (version 2.2023). URL: htps:/www.nccn.org.
19. Sands J, Tammemägi MC, Couraud S, et al. Lung screening benefits and challenges: A review of the data and outline for implementation. J Thorac Oncol, 2021, 16(1): 37-53.
20. 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, 2017, 18(11): 1523-1531.
21. Jha P, Peto R. Global effects of smoking, of quitting, and of taxing tobacco. N Engl J Med, 2014, 370(1): 60-68.
22. Office of the Surgeon General (US), Office on Smoking and Health (US). The Health Consequences of Smoking: A Report of the Surgeon General. Atlanta (GA): Centers for Disease Control and Prevention (US), 2004.
23. Darby S, Hill D, Auvinen A, et al. Radon in homes and risk of lung cancer: Collaborative analysis of individual data from 13 European case-control studies. BMJ, 2005, 330(7485): 223.
24. Driscoll T, Nelson DI, Steenland K, et al. The global burden of disease due to occupational carcinogens. Am J Ind Med, 2005, 48(6): 419-431.
25. Loomis D, Guha N, Hall AL, et al. Identifying occupational carcinogens: An update from the IARC Monographs. Occup Environ Med, 2018, 75(8): 593-603.
26. Delva F, Margery J, Laurent F, et al. Medical follow-up of workers exposed to lung carcinogens: French evidence-based and pragmatic recommendations. BMC Public Health, 2017, 17(1): 191.
27. O'Dwyer E, Halpenny DF and Ginsberg MS. Lung cancer screening in patients with previous malignancy: Is this cohort at increased risk for malignancy? Eur Radiol, 2021, 31(1): 458-467.
28. Wu GX, Nelson RA, Kim JY, et al. Non-small cell lung cancer as a second primary among patients with previous malignancy: Who is at risk? Clin Lung Cancer, 2017, 18(5): 543-550.
29. Yang IA, Holloway JW, Fong KM. Genetic susceptibility to lung cancer and co-morbidities. J Thorac Dis, 2013, 5 (Suppl 5): S454-S462.
30. Hubbard R, Venn A, Lewis S, et al. Lung cancer and cryptogenic fibrosing alveolitis. A population-based cohort study. Am J Respir Crit Care Med, 2000, 161(1): 5-8.
31. Coté ML, Liu M, Bonassi S, et al. Increased risk of lung cancer in individuals with a family history of the disease: A pooled analysis from the International Lung Cancer Consortium. Eur J Cancer, 2012, 48(13): 1957-1968.
32. Tammemägi MC, Katki HA, Hocking WG, et al. Selection criteria for lung-cancer screening. N Engl J Med, 2013, 368(8): 728-736.
33. Tammemägi MC, Church TR, Hocking WG, et al. Evaluation of the lung cancer risks at which to screen ever- and never-smokers: Screening rules applied to the PLCO and NLST cohorts. PLoS Med, 2014, 11(12): e1001764.
34. Pasquinelli MM, Tammemägi MC, Kovitz KL, et al. Risk prediction model versus united states preventive services task force lung cancer screening eligibility criteria: Reducing race disparities. J Thorac Oncol, 2020, 15(11): 1738-1747.
35. Tammemägi MC, Ten Haaf K, Toumazis I, et al. Development and validation of a multivariable lung cancer risk prediction model that includes low-dose computed tomography screening results: A secondary analysis of data from the National Lung Screening Trial. JAMA Netw Open, 2019, 2(3): e190204.
36. McWilliams A, Tammemagi MC, Mayo JR, et al. Probability of cancer in pulmonary nodules detected on first screening CT. N Engl J Med, 2013, 369(10): 910-919.
37. Yang D, Liu Y, Bai C, et al. Epidemiology of lung cancer and lung cancer screening programs in China and the United States. Cancer Lett, 2020, 468: 82-87.
38. Marshall HM, Bowman RV, Yang IA, et al. Screening for lung cancer with low-dose computed tomography: A review of current status. J Thorac Dis, 2013, 5 (Suppl 5): S524-S539.
39. Christenson SA, Smith BM, Bafadhel M, et al. Chronic obstructive pulmonary disease. Lancet, 2022, 399(10342): 2227-2242.
40. Gould MK, Donington J, Lynch WR, et al. Evaluation of individuals with pulmonary nodules: When is it lung cancer? Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest, 2013, 143(5 Suppl): e93S-e120S.
41. Kazerooni EA, Armstrong MR, Amorosa JK, et al. ACR CT accreditation program and the lung cancer screening program designation. J Am Coll Radiol, 2016, 13(2 Suppl): R30-R34.
42. Gardiner N, Jogai S, Wallis A. The revised lung adenocarcinoma classification: An imaging guide. J Thorac Dis, 2014, 6(Suppl 5): S537-S546.
43. Naidich DP, Bankier AA, MacMahon H, et al. Recommendations for the management of subsolid pulmonary nodules detected at CT: A statement from the Fleischner Society. Radiology, 2013, 266(1): 304-317.
44. Patz EF Jr , Greco E, Gatsonis C, et al. Lung cancer incidence and mortality in National Lung Screening Trial participants who underwent low-dose CT prevalence screening: A retrospective cohort analysis of a randomised, multicentre, diagnostic screening trial. Lancet Oncol, 2016, 17(5): 590-599.
45. 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, 2017, 72(9): 819-824.
46. Detterbeck FC, Bolejack V, Arenberg DA, et al. The IASLC Lung Cancer Staging Project: Background data and proposals for the classification of lung cancer with separate tumor nodules in the forthcoming eighth edition of the TNM classification for lung cancer. J Thorac Oncol, 2016, 11(5): 681-692.
47. de Koning HJ, van der Aalst CM, de Jong PA, et al. Reduced lung-cancer mortality with volume CT screening in a randomized trial. N Engl J Med, 2020, 382(6): 503-513.
48. Pastorino U, Silva M, Sestini S, et al. Prolonged lung cancer screening reduced 10-year mortality in the MILD trial: New confirmation of lung cancer screening efficacy. Ann Oncol, 2019, 30(7): 1162-1169.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Interpretation of the NCCN clinical practice guidelines in oncology for lung cancer screening (version 2.2023)

Abstract Full text Figures/Tables Video References Cited by

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