Changes in Uptake, Participant Disparities, and Screening Outcomes of the Korean National Lung Cancer Screening Program: A Five-Year Experience
Article information
Abstract
Purpose
Low-dose computed tomography (LDCT) is effective in reducing lung cancer mortality among high-risk smokers. The Korean National Lung Cancer Screening Program (KNLCS), the world’s first nationwide lung cancer screening initiative using LDCT, was launched in 2019. This study aimed to evaluate the KNLCS uptake rates in relation to participants’ economic status and changes in positive screening rates across screening rounds.
Materials and Methods
Data from the National Health Insurance Service (NHIS) and the National Cancer Screening Information System for 2019-2023 were analyzed. Eligible participants in the KNLCS were current smokers aged 54-74 years with a smoking history of at least 30 pack-years. The KNLCS provides counseling by physicians on screening results and smoking cessation. Screening uptake rates, counseling rates, and Lung CT Screening Reporting and Data System (Lung-RADS) distributions were assessed.
Results
Screening uptake rates increased from 24.7% in 2019 to 51.2% in 2023 (p < 0.001). Economic disparities were observed, with higher-income groups showing consistently higher uptake rates than lower-income groups. Screening positive rates have decreased from 9.1% in 2019 to 7.0% in 2023 due to the increasing proportion of subsequent screening participants. The interinstitutional variance in Lung-RADS category 4 decreased significantly over the years (p < 0.001).
Conclusion
The KNLCS rapidly increased screening uptake rates by systematically inviting eligible participants. Positive screening rates decreased primarily due to a reduction in Lung-RADS category 3 findings in subsequent rounds.
Introduction
Lung cancer is the leading cause of cancer-related deaths in South Korea [1]. The efficacy of low-dose computed tomography (LDCT) in lung cancer screening has been well established through landmark randomized controlled trials, including the National Lung Screening Trial (NLST) [2] and the Dutch-Belgian lung cancer screening trial (NELSON) [3], which demonstrated significant reductions in lung cancer mortality rates [4,5].
Based on the evidence supporting LDCT screening, South Korea published guidelines in 2015 recommending lung cancer screening using LDCT for high-risk individuals [6]. This led to the Korean Lung Cancers Screening Project (K-LUCAS), a nationwide, multi-center study to assess the feasibility of a national screening program [7]. Based on K-LUCAS findings, South Korea implemented the world’s first nationwide lung cancer screening program in 2019, targeting current smokers aged 54-74 years with at least 30 pack-years of smoking history.
The National Health Insurance Service (NHIS) selects eligible individuals and sends invitation letters for the Korean National Lung Cancer Screening Program (KNLCS), which provides LDCT screening biannually and counseling for screening results and smoking cessation. Screening costs are fully covered for individuals in the lower 50% income bracket or those eligible for Medical Aid, while others pay only 10% out-of-pocket. The screening program is conducted at designated general hospitals that meet specific criteria, including the presence of trained radiologists, possession of a 16-row or higher computed tomography (CT) scanner, and trained physicians to provide screening results and smoking cessation counseling. The KNLCS mandates LDCT with a CTDIvol (computed tomography dose index volume) ≤ 3 mGy and a section thickness of less than 1.5 mm. Screening results are reported using the Lung CT Screening Reporting and Data System (Lung-RADS) [8]. In the KNLCS, categories 3 and 4 are considered positive results that require further evaluation.
The KNLCS periodically monitors screening uptake and positive results using the National Cancer Screening Information System (NCSIS), established at the National Cancer Center Korea (NCCK). This system allows for the continuous tracking and analysis of screening outcomes, providing feedback for quality control in participating hospitals.
This study aimed to report the uptake and positive screening rates of the KNLCS for 5 years from 2019 to 2023. Additionally, it investigated changes in screening uptake rates related to the economic status and Lung-RADS distribution of the participants across screening rounds. Through this analysis, we sought to provide valuable insights into the effectiveness of large-scale population-based lung cancer screening programs and identify potential areas for improvement, contributing to efforts to reduce lung cancer mortality in South Korea, and to inform similar initiatives globally.
Materials and Methods
1. Data source
This study utilized two primary data sources: the NHIS [9] and the NCSIS databases [10]. The NHIS, the only mandatory insurer for universal healthcare in South Korea, covers nearly all citizens and provides the majority of funding for the KNLCS. The NHIS selects an eligible target population for the KNLCS and sends invitation letters to high-risk individuals. After screening, the hospitals send the results to participants and report them to the NHIS for reimbursement of screening costs. The NCSIS, established at the NCCK, provides financial support for out-of-pocket expenses and screening results in the National Cancer Screening Program (NCSP), encompassing data on NHIS beneficiaries within the lower 50% insurance premium bracket and Medical Aid recipients. To analyze changes in Lung-RADS distribution, we utilized the NCSIS database, which provides comprehensive screening data for the target population. Insurance premiums, determined by household income and assets, were included in the analysis as proxies for the economic status of the participants.
2. Study population
Our study targeted individuals eligible for KNLCS from 2019 to 2023—current smokers aged 54 to 74 years with a minimum smoking history of 30 pack-years, as verified through the National Health Screening Program [9] or National Smoking Cessation Service [11]. From 2019 to 2023, the number of lung cancer screening institutes increased from 279 to 319. Because the estimated positive screening rates from institutions with insufficient cases may be inaccurate, only institutes that performed more than 100 LDCT screenings in the relevant year in the NCSIS were included in the analysis of the variability of positive rates. The annual Lung-RADS distributions from institutions performing fewer than 100 screenings are presented in S1 Table. These accounted for 8.6% of all screenings in 2019 (n=4,459) and 2.2% in 2023 (n=2,027), showing a consistently decreasing proportion over time.
3. Statistical analysis
Descriptive statistics were used to summarize the characteristics of the study population and screening outcomes. Trends in screening uptake rates, positive rates, and consultant visit rates over the years 2019-2023 were analyzed using the Cochran-Armitage test. To assess differences in screening uptake rates and counseling rates across insurance premium categories, a quasi-Poisson regression model was applied. The variability in positive rates across different years was compared by calculating the coefficient of variation (CV), defined as the standard deviation divided by the mean. To further compare the variability in positivity rates among screening institutes by year, the CV by year was compared using the Bennett test [12].
All statistical analyses were performed using R ver. 4.4.1 (R Foundation for Statistical Computing). Statistical significance was set at p < 0.05.
Results
The KNLCS showed a consistent increase in the screening uptake rates from 2019 to 2023 (Table 1). Screening uptake increased from 82,018 (24.7%) in 2019 to 166,255 (51.2%) in 2023 (p < 0.001). Concurrently, the positive rates (Lung-RADS categories 3 and 4) decreased from 9.1% in 2019 to 7.0% in 2023 (p < 0.001).
Table 2 presents the screening uptake and counseling rates of the KNLCS stratified by insurance premiums as a proxy for economic status. From 2021 onward, the upper 50% premium group consistently showed higher screening uptake rates than both the lower 50% premium and Medical Aid groups. The difference in screening uptake rates between economic status groups remained consistent, even after adjusting for the increasing trend over the screening years. Compared to the upper 50% premium group, the screening uptake rate for the Medical Aid group was 0.62 times lower (95% confidence interval, 0.38 to 0.95). Although the proportion of visits for counseling on screening results was consistently highest in the Medical Aid group from 2019 to 2023, the differences in counseling visit rates across economic groups were not statistically significant after adjusting for the screening year.
National Lung Cancer Screening Program results in South Korea according to insurance premium as a proxy for economic status, 2019-2023
Table 3 summarizes the distribution of Lung-RADS categories across the first and subsequent screening rounds. The proportion of participants undergoing subsequent rounds increased from 22.8% in 2021 to 38.2% in 2023, and the proportion of those screened again at the same institution rose from 16.5% to 34.2% during the same period. Regarding Lung-RADS category 3, subsequent rounds performed at the same institution consistently showed lower proportions compared with the initial screening (2.2% vs. 5.4% in 2021, 2.0% vs. 4.2% in 2022, and 2.4% vs. 4.3% in 2023). By contrast, subsequent rounds performed at different institutions showed higher proportions of category 3 than the first round (5.5% vs. 5.4% in 2021, 5.0% vs. 4.2% in 2022, and 4.6% vs. 4.3% in 2023).
National Lung Cancer Screening Program results according to screening rounds in South Korea, 2019-2023
Table 4 shows dynamics in the Lung-RADS categories among the first and subsequent rounds. Participants with lower Lung-RADS categories in previous screenings had a substantially reduced risk of receiving positive results in subsequent screenings. Of those initially classified as category 1, only 4.7% progressed to category 3 or 4 in the second round. For those who were initially in category 2, 7.5% progressed to category 3 or 4. Conversely, 15.6% of those initially in category 3 and 19.6% of those in category 4 remained positive in subsequent screening rounds. The distribution of the Lung-RADS categories across three consecutive rounds of screening from 2019 to 2023 showed that the proportion of patients in category 4 remained relatively stable, at approximately 3.6%-3.8%, across all rounds (S2 Table).
Table 5 presents the variability in the proportion of positive results among lung cancer screening institutes from 2019 to 2023. For Lung-RADS categories 3 or 4, CV in the proportion of positive rates also decreased; however, no significant differences were shown across the years. The overall CV, as well as those for the first and subsequent screening rounds, were 0.58, 0.61, and 0.79 respectively, in 2021; and 0.63, 0.64, and 0.73, respectively, in 2022. The p-values of 0.093, 0.448, and 0.083 indicate that the variability in this category remained relatively stable over time. Conversely, for Lung-RADS category 4, there were significant differences in the variability of positive rates across years. The overall p-value was less than 0.001, and the p-values for the first and subsequent screening rounds were 0.881 and less than 0.001, respectively. This significant decrease in variability suggests an improvement in the uniformity of high-risk classification across different screening centers.
Discussion
This study presented the first comprehensive analysis of screening uptake rates and Lung-RADS distribution across multiple screening rounds in a nationwide organized lung cancer screening program, which currently provides biennial LDCT screening. Our findings demonstrate a rapid increase in lung cancer screening rates in South Korea, with a notable decrease in positive rates during subsequent screening rounds, particularly when subsequent screenings were performed at the same institution, largely driven by a reduction in Lung-RADS category 3 classifications. Additionally, a significant reduction in variability for Lung-RADS category 4 suggests improved consistency in high-risk classifications across screening centers.
The KNLCS, introduced in the latter half of 2019, has shown remarkable progress, with annual screening uptake rates rising from 24.7% in 2019 to 51.2% in 2023. Despite the initial launch of the KNLCS, the increase in uptake rates was minimal between 2019 (24.7%) and 2020 (25.8%). This limited growth can likely be attributed to reduced healthcare utilization during the coronavirus diseases 2019 pandemic, which is consistent with the reported decrease in screening uptake rates for other cancers within the NCSP [13] and the decline in confirmed cancer cases reported in the Korean Cancer Registry [1] during the same period. Nevertheless, the overall achievement of uptake rates surpasses those observed in similar lung cancer screening programs. In the United States, despite the recommendation for lung cancer screening starting in 2013 [5], the uptake rate remained below 20% in 2019 [14], and only reached 5.8% in 2021 even after expanding eligibility criteria [15]. Similarly, in Canada, the cumulative uptake rate from 2015 to 2018 was only 6.0% [16]. In China, a lung cancer screening program was first introduced in certain rural provinces in 2010. According to the National Lung Cancer Screening Cohort [17], the cumulative screening rate from 2013 to 2018 was 33.0%. In Japan, where lung cancer screening with chest radiography and sputum cytology was introduced nationwide in 1987 [18], the uptake rates in 2019 were 53.4% for men and 45.6% for women [19]. Meanwhile, the screening uptake rates in South Korea in 2019 and 2020 were reported to be approximately 23% [20], which is slightly lower than the 24.7% and 25.8% we reported in 2019 and 2020, respectively. When defining an eligible population during the process of extracting data from the NHIS, the estimate of uptake rates may differ in the process of excluding dead or overseas residents.
Several factors may have contributed to the high uptake rate of lung cancer screening in South Korea. First, the program effectively utilized the existing infrastructure established for cancer screening through the NCSP, which is organized at a nationwide level [21]. Second, the identification of the eligible population for the KNLCS was efficiently facilitated by leveraging existing databases. The NHIS maintains comprehensive data on smoking history collected through the National Health Screening and National Smoking Cessation Programs. Third, the cost structure of the NCSP plays a crucial role in facilitating high participation. The program’s design ensures no out-of-pocket expenses for individuals in the lower 50% of the insurance premium bracket and Medicaid Aid recipients, whereas those outside these categories pay only a minimal 10% out-of-pocket cost [22].
However, our findings revealed significant disparities in screening uptake and outcomes across the different economic groups. Although lung cancer screening rates have increased in all insurance premium categories, the disparities across these categories were increasing. Similar to our results, inequality according to income level has been reported in stomach, breast, and cervical cancer screening uptake [23,24]. This disparity highlights the need for targeted interventions to improve access and participation in lower-income groups.
The rate of repeated participation in screening programs has increased annually. This trend highlights the high adherence to the nationwide organized cancer screening program. Increased repeat participation is expected to reduce the need for follow-up examinations, enhancing the cost-effectiveness of the lung cancer screening program. The observed decrease in positive rates in subsequent screening rounds in the KNLCS from 2019 to 2023, primarily due to fewer Lung-RADS category 3 findings, suggests improved diagnostic precision and reduced unnecessary follow-ups, aligning with previous studies. In the NELSON trial [25], the proportion of positive results (indeterminate or positive nodule management of NELSON trial) decreased from 20.8% in the first round to 7.8% and 8.1% in the second and third rounds, respectively. A French cohort study also reported a decrease in the proportion of positive results from 23.1% in the first round to 8.0% in the second round, with the proportion of indeterminate findings (equivalent to category 3 in Lung-RADS) decreasing from 18.0% to 3.4% [26]. Lung-RADS categorizes lung cancer risk, allowing many stable lesions to be classified without the need for follow-up examinations in subsequent rounds. These findings align with previous observations in the NLST [27].
In our study, the positivity rate decreased from 9.1% in 2019 to 7.0% in 2022 and 2023. This decrease in positive rates can be attributed to two primary factors. First, when nationwide mass screening was initially introduced, symptomatic patients may have been more likely to be included in the early screening rounds, which was observed when the NCSP first implemented the gastric cancer screening program [28]. Second, the proportion of participants undergoing subsequent screening rounds increased. As described above, the proportion of patients in Lung-RADS category 3 decreased in the subsequent screening rounds. Nevertheless, the positive rates among those who underwent subsequent screening rounds in 2021 were higher than those in 2022 and 2023. This could indicate that participants at the initial screening had a relatively high lung cancer risk or that radiologists may have been more cautious in interpreting LDCT results, leading to higher positive rates. To confirm these assumptions, it is necessary to focus on variables such as the medical history of the participants and differences in diagnostic accuracy related to radiologist experience in interpreting LDCT results.
Our study had several limitations. First, the changes in lung lesions according to the screening rounds reported in the Lung-RADS could not be identified. Therefore, the progression of individual lung lesions into cancer remains unknown. However, the NELSON trial reported that new nodules had a much higher probability of developing lung cancer than baseline nodules [29]. Second, we lacked detailed information on screening results based on age or socioeconomic factors beyond insurance premium categories. Because the lung cancer screening program primarily targets high-risk individuals identified using smoking history data from the NHIS, the NCSIS does not provide granular data on the characteristics of screened participants or those who did not participate in the program. Third, this study did not include data on early-stage lung cancers detected through LDCT screening, nor did it provide information on screening accuracy. Addressing this limitation requires further evaluation through linking cancer registry data with screening outcome databases to enable a more comprehensive assessment of the program’s effectiveness. Finally, institutions performing fewer than 100 annual screenings were excluded from the analysis of inter-institutional variation because the proportions of Lung-RADS categories 3 and 4 could be unstable with limited case numbers. Although low-volume screening is known to raise concerns regarding quality management [30], such institutions accounted for only 2.2% of all screenings in 2023, suggesting minimal impact on the main results.
South Korea’s national lung cancer screening program has achieved a significant increase in the uptake rates through a well-organized nationwide system. The decline in screening positive rates over time, particularly in Lung-RADS category 3 findings, suggests enhanced efficiency in reducing false positives that would otherwise lead to unnecessary follow-up examinations. However, economic disparities in screening uptake and the decreasing proportion of participants receiving counseling raise concerns about reduced compliance with further evaluations of positive findings and insufficient interventions to support smoking cessation. Future research should prioritize evaluating the program’s impact on smoking cessation rates, early lung cancer detection, and mortality reduction in the screened population. Additionally, targeted strategies are required to mitigate socioeconomic disparities and enhance diagnostic accuracy in screening participation.
Electronic Supplementary Material
Supplementary materials are available at Cancer Research and Treatment website (https://www.e-crt.org).
Notes
Ethical Statement
This study was conducted in accordance with the Declaration of Helsinki. The study analyzed anonymized national cancer screening data and was approved by the Institutional Review Board (IRB) of the NCCK (IRB No. NCC2024-0177).
Author Contributions
Conceived and designed the analysis: Choi CK, Kim Y.
Collected the data: Suh M, Choi KS, Kim Y.
Contributed data or analysis tools: Suh M, Choi KS, Kim Y.
Performed the analysis: Choi CK, Lee NY.
Wrote the paper: Choi CK, Suh M, Choi KS, Kim Y.
Conflicts of Interest
Conflict of interest relevant to this article was not reported.
Funding
This study was supported by research grants (NCC-2210810 to Y. Kim and NCC-2410700 to C.K. Choi) from National Cancer Center, Republic of Korea, and grant (NCC-2460030 to Y. Kim) from the Quality Control Program for the National Cancer Screening Program, Ministry of Health and Welfare, Republic of Korea.
