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• W4377016776 abstract "There is no doubt that screening is the most efficient strategy for controlling cancer in addition to prevention. Lung cancer is responsible for the largest global cancer burden in 2020, being the second most common and deadliest malignancy worldwide.1Sung H. Ferlay J. Siegel R.L. 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: 209-249Crossref PubMed Scopus (30236) Google Scholar Several clinical trials have been conducted since the 1970s to determine the usefulness of chest radiographs, with or without sputum cytology, as a screening tool for lung cancer.2Artinian V. Kvale P.A. Update in screening of lung cancer.Respirology. 2005; 10: 558-566Crossref PubMed Scopus (9) Google Scholar Unfortunately, all clinical trials have failed, indicating that not only annual but also four-monthly chest radiographs are useless. Thanks to the development of low-dose computed tomography (LDCT) in the 1990s, two large randomized controlled trials (National Lung Screening Trial [NLST] and Nederlands–Leuvens Longkanker Screenings Onderzoek [NELSON]) were initiated in the early 2000s, and it was finally proven that LDCT can substantially reduce lung cancer mortality by up to 20%.3Aberle D.R. Adams A.M. et al.National Lung Screening Trial Research TeamReduced lung-cancer mortality with low-dose computed tomographic screening.N Engl J Med. 2011; 365: 395-409Crossref PubMed Scopus (7124) Google Scholar,4de Koning H.J. van der Aalst C.M. de Jong P.A. et al.Reduced lung-cancer mortality with volume CT screening in a randomized trial.N Engl J Med. 2020; 382: 503-513Crossref PubMed Scopus (1262) Google Scholar The reduction of lung cancer mortality in NLST and NELSON was mainly because screening increased the proportion of stage I disease from 24% to around 60%. The real-world evidence also supports the stage shift by screening, which can detect patients with lung cancer in earlier curable stages, as the most effective way to improve lung cancer survival.5Yang C.Y. Lin Y.T. Lin L.J. et al.Stage shift improves lung cancer survival: real-world evidence.J Thorac Oncol. 2023; 18: 47-56Abstract Full Text Full Text PDF Scopus (6) Google Scholar Although tobacco is the single most important and well-known carcinogen contributing to lung cancer, many lung cancers occur in patients who did not have a smoking history. The global incidence of lung cancer in never-smokers (LCNS) is increasing.1Sung H. Ferlay J. Siegel R.L. 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: 209-249Crossref PubMed Scopus (30236) Google Scholar The true global impact of LCNS is not clear because smoking history is not captured in most cancer registry databases. However, it has been estimated that LCNS would rank seventh leading cause of cancer mortality worldwide, and at least one-third of patients with lung cancer did not have a smoking history.1Sung H. Ferlay J. Siegel R.L. 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: 209-249Crossref PubMed Scopus (30236) Google Scholar,6Sun S. Schiller J.H. Gazdar A.F. Lung cancer in never smokers—a different disease.Nat Rev Cancer. 2007; 7: 778-790Crossref PubMed Scopus (1162) Google Scholar This estimation was on the basis of Global Cancer Statistics and the smoking prevalence of patients with lung cancer in the literature. If lung cancer screening only focuses on heavy smokers, there will be more than 30% of patients with lung cancer not screened. Expanding screening eligibility to cover never-smokers with lung cancer risk is the most urgent unmet need to improve global lung cancer control. Asia has the most serious disease burden of lung cancer globally, with nearly 59% of the world's lung cancer incidence and 61% of lung cancer mortality occurring in Asia.7International Agency for Research on Cancer, World Health Organization Global Cancer Observatorycancer today.https://gco.iarc.fr/todayDate accessed: March 9, 2023Google Scholar LCNS has a higher prevalence and is more serious in East Asia.5Yang C.Y. Lin Y.T. Lin L.J. et al.Stage shift improves lung cancer survival: real-world evidence.J Thorac Oncol. 2023; 18: 47-56Abstract Full Text Full Text PDF Scopus (6) Google Scholar,7International Agency for Research on Cancer, World Health Organization Global Cancer Observatorycancer today.https://gco.iarc.fr/todayDate accessed: March 9, 2023Google Scholar The age-standardized mortality of lung cancer is also highest in East Asia.7International Agency for Research on Cancer, World Health Organization Global Cancer Observatorycancer today.https://gco.iarc.fr/todayDate accessed: March 9, 2023Google Scholar Lung cancer in smokers (LCS) and LCNS are two different diseases. The molecular pathogenesis, genetic susceptibility, and environmental risk factors are different,8Chen Y.J. Roumeliotis T.I. Chang Y.H. et al.Proteogenomics of non-smoking lung cancer in East Asia delineates molecular signatures of pathogenesis and progression.Cell. 2020; 182: 226-244.e17Abstract Full Text Full Text PDF PubMed Scopus (116) Google Scholar and implicating lung cancer control programs may need to have different considerations. In Taiwan, although smoking prevalence has decreased progressively in the past three decades, the incidence of lung cancer continues to increase. Currently, the prevalence of smoking in patients with lung cancer is 33.7% (62.8% in men and 5.9% in women), and more than 50% of patients with lung cancer are stage III and IV diseases at diagnosis. This indicates that lung cancer control in Taiwan may need a different strategy and it is necessary to develop a screening strategy focusing on both heavy smokers and never-smokers.9Tseng C.H. Tsuang B.J. Chiang C.J. et al.The relationship between air pollution and lung cancer in nonsmokers in Taiwan.J Thorac Oncol. 2019; 14: 784-792Abstract Full Text Full Text PDF PubMed Scopus (91) Google Scholar, 10Lo Y.L. Hsiao C.F. Chang G.C. et al.Risk factors for primary lung cancer among never smokers by gender in a matched case-control study.Cancer Causes Control. 2013; 24: 567-576Crossref PubMed Scopus (50) Google Scholar, 11Health promotion administration annual reportMinistry of Health and Welfare, Taiwan Cancer Registry.https://www.hpa.gov.tw/EngPages/List.aspx?nodeid=1070Date accessed: May 30, 2022Google Scholar Because of increased awareness, smoking history has become a required item in Taiwan's national cancer registry since 2011, making it possible to directly address the importance of LCNS. In 2020, when divided by smoking status, LCNS would rank sixth in incidence, and LCS would rank ninth. In terms of mortality, LCNS and LCS would rank fifth and fourth, respectively. For women, the situation is even more concerning: LCNS would rank third in both incidence and mortality. These numbers highlight the critical situation of LCNS in this region and urge society to take action.11Health promotion administration annual reportMinistry of Health and Welfare, Taiwan Cancer Registry.https://www.hpa.gov.tw/EngPages/List.aspx?nodeid=1070Date accessed: May 30, 2022Google Scholar LDCT has been found to be an effective screening tool for heavy smokers, but its usefulness in never-smokers has been controversial until now. Triphuridet et al.,12Triphuridet N. Zhang S.S. Nagasaka M. et al.Low-dose computed tomography (LDCT) lung cancer screening in Asian female never-smokers is as efficacious in detecting lung cancer as in Asian male-ever-smokers: a systematic review and meta-analysis.J Thorac Oncol. 2023; 18: 698-717Abstract Full Text Full Text PDF Scopus (3) Google Scholar in this issue of the Journal of Thoracic Oncology, reported a meta-analysis evaluating the effectiveness of LDCT screening in never-smokers. The meta-analysis included 14 studies comprising 141,396 ever-smokers and 109,251 never-smokers, with the Asian population accounting for 79% of the study population. In total, 1961 lung cancer cases were identified, with 1172 in ever-smokers (0.83%) and 789 in never-smokers (0.72%). The primary objective of this study was to compare the relative risk (RR) of lung cancer detection by LDCT between ever-smokers and never-smokers, and the authors found no significant difference (RR = 1.21, 95% confidence interval [CI]: 0.89–1.65). The study results suggested that the risk of lung cancer detected by LDCT in Asian female never-smokers was similar to that of overall high-risk ever-smokers (≥30 pack-years) (RR = 0.99, 95% CI: 0.65–1.50). Furthermore, the study suggested that LDCT was more effective in reducing lung cancer mortality in never-smokers than in ever-smokers (RR = 0.27, 95% CI: 0.1–0.55). To our knowledge, this is the first large meta-analysis that provides evidence suggesting the benefits of LDCT lung cancer screening in never-smokers. Most previous analyses were against the application of LDCT screening in patients without a smoking history. The major reason for the different conclusions likely lies in the study population. It is generally agreed that a risk-based screening program is more effective. However, the database from which the risk model is developed will determine the limitations of the model. The lung cancer risk prediction model PLCOall2014,13Tammemägi M.C. Church T.R. Hocking W.G. 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; 11e1001764Crossref PubMed Scopus (221) Google Scholar a modification from the PLCOm2012 model, and the Microsimulation Screening Analysis–Lung microsimulation model14Ten Haaf K. de Koning H.J. Should never-smokers at increased risk for lung cancer be screened?.J Thorac Oncol. 2015; 10: 1285-1291Abstract Full Text Full Text PDF PubMed Scopus (26) Google Scholar are two well-known risk models that were developed from the Prostate, Lung, Colorectal, and Ovarian (PLCO), NLST, and the Surveillance, Epidemiology, and End Results databases in the United States. Both of these models do not recommend LDCT screening in never-smokers. However, only 3.6% of the participants in PLCO, 2% in NLST, and 6% in the Surveillance, Epidemiology, and End Results databases were Asian.3Aberle D.R. Adams A.M. et al.National Lung Screening Trial Research TeamReduced lung-cancer mortality with low-dose computed tomographic screening.N Engl J Med. 2011; 365: 395-409Crossref PubMed Scopus (7124) Google Scholar,15Oken M.M. Hocking W.G. Kvale P.A. et al.Screening by chest radiograph and lung cancer mortality: the Prostate, Lung, Colorectal, and Ovarian (PLCO) randomized trial.JAMA. 2011; 306: 1865-1873Crossref PubMed Scopus (501) Google Scholar,16Hamid M.S. Shameem R. Gafoor K. George J. Mina B. Sullivan K. Non-small-cell lung cancer clinicopathologic features and survival outcomes in Asian pacific islanders residing in the United States: a SEER analysis.J Cancer Epidemiol. 2015; 2015269304Crossref PubMed Scopus (11) Google Scholar Several models have similar limitations (Table 1). On the other hand, in the current meta-analysis, 79% of the patients included were Asian, and 13 of the 14 studies were conducted in East Asia (People’s Republic of China, Japan, Korea, and Taiwan). Therefore, the present study results by Triphuridet et al.12Triphuridet N. Zhang S.S. Nagasaka M. et al.Low-dose computed tomography (LDCT) lung cancer screening in Asian female never-smokers is as efficacious in detecting lung cancer as in Asian male-ever-smokers: a systematic review and meta-analysis.J Thorac Oncol. 2023; 18: 698-717Abstract Full Text Full Text PDF Scopus (3) Google Scholar should be regarded as an augmentation rather than a conflict with previous studies. In contrast, it should also be noted that whether the conclusion of this study applies to Asian descendants outside Asia is yet to be determined.Table 1Lung Cancer Risk Prediction ModelReferenceBach18Bach P.B. Kattan M.W. Thornquist M.D. et al.Variations in lung cancer risk among smokers.J Natl Cancer Inst. 2003; 95: 470-478Crossref PubMed Scopus (496) Google ScholarSpitz19Spitz M.R. Hong W.K. Amos C.I. et al.A risk model for prediction of lung cancer.J Natl Cancer Inst. 2007; 99: 715-726Crossref PubMed Scopus (324) Google ScholarLLP20Cassidy A. Myles J.P. van Tongeren M. et al.The LLP risk model: an individual risk prediction model for lung cancer.Br J Cancer. 2008; 98: 270-276Crossref PubMed Scopus (341) Google ScholarTSCE21Meza R. Hazelton W. Colditz G. Moolgavkar S. Analysis of lung cancer incidence in the Nurses’ Health and the Health Professionals’ Follow-Up Studies using a multistage carcinogenesis model.Cancer Causes Control. 2008; 19: 317-328Crossref PubMed Scopus (81) Google ScholarPLCOall201413Tammemägi M.C. Church T.R. Hocking W.G. 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; 11e1001764Crossref PubMed Scopus (221) Google ScholarMISCAN14Ten Haaf K. de Koning H.J. Should never-smokers at increased risk for lung cancer be screened?.J Thorac Oncol. 2015; 10: 1285-1291Abstract Full Text Full Text PDF PubMed Scopus (26) Google ScholarWu22Wu X. Wen C.P. Ye Y. et al.Personalized Risk Assessment in Never, Light, and Heavy Smokers in a prospective cohort in Taiwan.Sci Rep. 2016; 636482Google ScholarWarkentin23Warkentin M.T. Lam S. Hung R.J. Determinants of impaired lung function and lung cancer prediction among never-smokers in the UK Biobank cohort.EBiomedicine. 2019; 47: 58-64Abstract Full Text Full Text PDF PubMed Scopus (17) Google ScholarChien24Chien L.H. Chen C.H. Chen T.Y. et al.Predicting lung cancer occurrence in never-smoking females in Asia: TNSF-SQ, a prediction model.Cancer Epidemiol Biomarkers Prev. 2020; 29: 452-459Crossref PubMed Scopus (16) Google ScholarGuo25Guo L.W. Lyu Z.Y. Meng Q.C. et al.Construction and validation of a lung cancer risk prediction model for non-smokers in China.Front Oncol. 2022; 11766939Crossref Scopus (8) Google ScholarYear2003200720082008201420152016201920202022PopulationAmerican (CARET)AmericanUK (Liverpool)American (NHS, HPFS)American (PLCO,NLST)American (PLCO, NLST, SEER)TaiwaneseUK (UK-biobank)TaiwaneseChineseTotal cases18,172--152,169154,900-395,875218,892-107,382Lung cancer1070185157916263316-11171651748158Matched control-20011157-----6535-Asian1.1%0%< 1%0%PLCO 3.6%, NLST 2%,SEER 6%100%3%100% (female)100%Never-smoker0%0%20.9%48.46%PLCO 45%, NLST 0%,SEER n.a.71%100%100%100%AUC-0.57 – 0.630.70-0.848-0.732 – 0.8470.694 –0.7220.7140.668 –0.685PredictorsAge, sex, smoking, asbestosSmoking, asbestos, family Hx, COPD, dust, hay feverAge, sex, smoking, asbestos, cancer Hx, family Hx, pneumoniaAge, sex, smokingAge, smoking, cancer Hx, family Hx, race, education, BMI, COPDAge, sex, smoking, dietAge, sex, family Hx, BMI, PF, AFP, CEAAge, sex, cancer Hx, family Hx, PFFamily Hx, education, BMI, COPD, SNPAge, sex, family Hx, education, TB, lipidemiaAFP, α-fetoprotein; AUC, area under the curve; BMI, body mass index; CARET, Carotene and Retinol Efficacy Trial; CEA, carcinoembryonic antigen; COPD, chronic obstructive pulmonary disease; Hx, history; HPFS, Health Professionals Follow-up Study; LLP, Liverpool Lung Project; MISCAN, Microsimulation Screening Analysis; NHS, Nurses’ Health Study; NLST, National Lung Screening Trial; PF, pulmonary function; PLCO, the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial; SEER, The Surveillance, Epidemiology, and End Results; SNP, single nucleotide polymorphism; TB, tuberculosis; TSCE, Two-Stage Clonal Expansion; UK, United Kingdom. Open table in a new tab AFP, α-fetoprotein; AUC, area under the curve; BMI, body mass index; CARET, Carotene and Retinol Efficacy Trial; CEA, carcinoembryonic antigen; COPD, chronic obstructive pulmonary disease; Hx, history; HPFS, Health Professionals Follow-up Study; LLP, Liverpool Lung Project; MISCAN, Microsimulation Screening Analysis; NHS, Nurses’ Health Study; NLST, National Lung Screening Trial; PF, pulmonary function; PLCO, the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial; SEER, The Surveillance, Epidemiology, and End Results; SNP, single nucleotide polymorphism; TB, tuberculosis; TSCE, Two-Stage Clonal Expansion; UK, United Kingdom. Meta-analyses have intrinsic limitations, which are unavoidable in the present study. The information on some important potential confounding factors is either incomplete or missing. For example, the quantity and duration of smoking, and the starting age and cessation period, are all factors that contribute to lung cancer risk. A binary classification may overlook the differences. Secondly, a family history of lung cancer, which is probably the single most important risk factor for LCNS, is only assessed in 0.3% of the patients included in this meta-analysis. Lastly, none of the studies enrolled were randomized trials, and many of them were retrospective observations. Some selection bias is inevitable. Several issues require further consideration before implementing lung cancer screening in never-smokers. First, as pointed out by Triphuridet et al.,12Triphuridet N. Zhang S.S. Nagasaka M. et al.Low-dose computed tomography (LDCT) lung cancer screening in Asian female never-smokers is as efficacious in detecting lung cancer as in Asian male-ever-smokers: a systematic review and meta-analysis.J Thorac Oncol. 2023; 18: 698-717Abstract Full Text Full Text PDF Scopus (3) Google Scholar the screening interval may need to be considered differently for smokers and never-smokers. Second, the nodule management plan may also differ because the genetic and biological behavior of smoking-related and nonsmoking-related lung cancer are distinct. Third, an independent cost-benefit analysis is necessary. Generally, screening recommendations involve a trade-off between risks and benefits. Several lung cancer risk models for never-smokers are available (Table 1), and a prospective study is needed to validate their usefulness and cost-effectiveness. The ongoing Taiwan Lung Cancer Screening in Never-Smoker Trial (TALENT), initiated in 2015, is an LDCT screening study conducted exclusively in never-smokers at risk.17Yang P. PS01.02 National Lung Cancer Screening Program in Taiwan: the TALENT study.J Thorac Oncol. 2021; 16: S58Abstract Full Text Full Text PDF Google Scholar The study included patients aged 55 to 75 years old with risk factors, including a family history of lung cancer, passive smoking, tuberculosis or chronic obstructive pulmonary disease, and high cooking fume exposure. The TALENT first-round results revealed a lung cancer detection rate of 2.65% and 96.5% of patients with lung cancer were in stage 0 to I.17Yang P. PS01.02 National Lung Cancer Screening Program in Taiwan: the TALENT study.J Thorac Oncol. 2021; 16: S58Abstract Full Text Full Text PDF Google Scholar The initial results are promising, and the conclusion awaits follow-up maturation. On the basis of the TALENT study, the Taiwan government initiated a nationwide biennial LDCT screening program for patients with lung cancer risk since July 1, 2022. The program included patients 50 to 74 years old with a more than 30-pack-year smoking history, who agree to quit smoking; women 45 to 74 years old and men 50 to 74 years old who have never smoked but have a lung cancer family history. The TALENT study and Taiwan's nationwide LDCT screening may help to provide evidence for the feasibility of LDCT screening in never-smokers with risk factors in the near future. We congratulate Triphuridet et al.12Triphuridet N. Zhang S.S. Nagasaka M. et al.Low-dose computed tomography (LDCT) lung cancer screening in Asian female never-smokers is as efficacious in detecting lung cancer as in Asian male-ever-smokers: a systematic review and meta-analysis.J Thorac Oncol. 2023; 18: 698-717Abstract Full Text Full Text PDF Scopus (3) Google Scholar on their work. This study provides strong signals to support LDCT lung cancer screening in never-smokers. However, we do not believe that the evidence is sufficient to recommend mass screening for female never-smokers in Asia at this time. More data from prospective studies and cost-effectiveness analyses are required. Nevertheless, we firmly believe that it is time for the scientific community to refrain from completely rejecting LDCT lung cancer screening for never-smokers and start considering expanding eligibility for screening never-smokers with lung cancer risk. Chao-Hua Chiu: Conceptualization, Data curation, Visualization, Writing—original draft. Pan-Chyr Yang: Conceptualization, Data curation, Validation, Visualization, Writing— review & editing, Supervision, Funding acquisition. This work was supported by grants from the National Science and Technology Council (MOST 111-2314-B-038-157, MOST 110-0210-01-22-02, 110-2314-B-002-282), Next-Generation Pathway of Taiwan Cancer Precision Medicine Program (AS-KPQ-107-TCPMP), National Taiwan University (NTU-CC-111L894101), Key and Novel Therapeutics Development Program for Major Diseases (AS-KPQ-111-KNT). The authors thank Dr. Chun-Ju Chiang from Taiwan Cancer Registry for data acquisition and support. Low-Dose Computed Tomography (LDCT) Lung Cancer Screening in Asian Female Never-Smokers Is as Efficacious in Detecting Lung Cancer as in Asian Male Ever-Smokers: A Systematic Review and Meta-AnalysisJournal of Thoracic OncologyVol. 18Issue 6PreviewLung cancer in never-smokers is the major cancer cause of death globally. We compared the efficacy of low-dose computed tomography (LDCT) lung cancer screening among never-smokers versus ever-smokers using systematic review and meta-analysis. 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