Impact of annual trend volume of low-dose computed tomography for lung cancer screening on overdiagnosis, overmanagement, and gender disparities

Characteristics of lung cancer patients recorded in the cancer registry (2008 to 2021)

Table 1 displays yearly LDCT screening volumes and annual lung cancer statistics from 2008 to 2021, sourced from the hospital's cancer registry. It includes data on age, gender, lifestyle habits, stage distribution, behavior codes, lung cancer deaths, and survival rates at 1, 5, and 10 years, alongside the annual volume of LDCT exams conducted. The behavior code for lung cancer cases is assigned as malignant histology, whether in situ or invasive, in accordance with the pathology status [18]. Over this timeframe, 3,251 individuals within the hospital-based cohort in the specified target population were identified as having lung cancer. The lung cancer detection rate through LDCT screenings has gradually increased, rising from 1.3% in 2008 to 12.7% in 2021. Following the implementation of extensive LDCT examinations, the annual number of LDCT screenings in the hospital-based cohort exhibited a steady increase, starting at 245 in 2008 and reaching a peak of 3,079 in 2021. This signifies a remarkable 16-fold increase compared with the baseline period, with the most substantial growth observed between 2008 and 2019. The annual screening volume decreased from 2020 to 2021 due to isolation measures related to the coronavirus disease 2019 outbreak in Taiwan [19, 20].

Table 1 Characteristics of all patients diagnosed with lung cancer between 2008 and 2021 by sex, age, and period during gradual implementation of low-dose computed tomography screening in the hospital-based cohort

Between 2008 and 2021, the proportion of male lung cancer patients declined gradually from 70.9% to 46.8%, while the percentage of female patients increased from 29.1% to 53.2% (Fig. 2). The average age of lung cancer diagnosis decreased from 69.05 ± 12.755 years in 2008 to 63.64 ± 11.481 years in 2021. Figure 3 displays a trend analysis of LDCT screening volumes and stage 0 lung cancer cases from 2008 to 2021: from 2008 to 2019, both increased, reflecting a positive correlation. A decline occurred in 2020 due to the COVID-19 outbreak, followed by a significant rise in 2021 as pandemic conditions eased, further highlighting the correlation. The data also show a consistent increase in the percentage of stage 0 cases from 2008 to 2019, mirroring the rise in LDCT screenings.

Fig. 2figure 2

Trends in LDCT examination volumes and percentage of Lung Cancer by Gender from 2008 to 2021

Fig. 3figure 3

Trends in LDCT examination volumes and number of stage 0 Lung Cancer from 2008 to 2021

However, from 2019 to 2020, owing to the impact of the coronavirus disease 2019 pandemic, both the LDCT screening volume and the percentage of stage 0 lung cancer cases decreased slightly. Only with the easing of the pandemic in 2020 to 2021, did both indicators show a gradual upward trend (Fig. 4). The number of stage 0 lung cancers was minimal during the period from 2008 to 2013, with only sporadic three cases detected due to limited screening. However, starting from 2014, with the increasing volume of screenings over the years, the count of stage 0 lung cancers rose from six in 2014 to fifty in 2021.

Fig. 4figure 4

Trends in LDCT examination volumes and percentage of stage 0 Lung Cancer from 2008 to 2021

Correlation between lung cancer registry trend and LDCT scan volume

In this hospital cohort study, we explored the relationship between evolving lung cancer characteristics and LDCT volumes. Notably, we observed negative correlations between the annual changes regarding age at lung cancer diagnosis and LDCT screening volume (r =  − 0.843, P < 0.001) and between the annual trend in lung cancer death rates and LDCT implementation (r =  − 0.778, P = 0.001). Furthermore, negative correlations were observed between the number and percentage of stage 3 lung cancer cases and annual LDCT screening volume (r =  − 0.637, P = 0.014 and r =  − 0.753, P = 0.002, respectively) shown in Table 2.

Table 2 Investigating the relationship between changes in lung cancer characteristics over time and the introduction of low-dose computed tomography in a hospital cohort

In summary, our analysis revealed several significant correlations. We found a positive association between the annual increase in diagnosed lung cancer cases and LDCT screening volume (r = 0.730, P = 0.003). Similarly, a positive relationship was observed between LDCT screening volume and 1, 5, and 10-year survival rates (r = 0.912, P < 0.001; r = 0.964, P < 0.001; and r = 0.939, P = 0.005; respectively). Furthermore, positive associations were noted between the number and proportion of stage 0 lung cancer cases and annual LDCT screenings volume (r = 0.747, P = 0.002 and r = 0.801, P = 0.001, respectively). Positive correlations were observed between the number and proportion of stage 1 cases and annual LDCT screenings volume (r = 0.861, P < 0.001 and r = 0.912, P < 0.001, respectively).

Data visualization for differential trend periods and gender effect

Figure 5 compares LDCT screening volumes and stage 0 lung cancer cases from 2008 to 2021 by gender. Males consistently underwent more LDCT screenings, but females consistently had more stage 0 diagnoses; both charts share the same y-axis scale. This highlights LDCT screening's greater impact in increasing stage 0 lung cancer cases in females compared to males.

Fig. 5figure 5

Trends in LDCT examination volumes and number of stage 0 Lung Cancer by gender from 2008 to 2021

Figure 6 shows the fluctuating trends in the impact of LDCT examination volumes on various stages of lung cancer over the different time periods, highlighting the corresponding changes in diverse age groups. For stage 0 lung cancer, the table reveals a progressive increase in the LDCT scan volume over time. Notably, from 2017 to 2020, a significantly more pronounced increase in the number of stage 0 lung cancer cases across various age groups was noted compared with the periods 2013 to 2016 and 2009 to 2012. Additionally, the grouping by age exhibited a normal distribution pattern centered around an average age of 50 years. Regarding the variation in stage 1 lung cancer cases, LDCT scan volumes increased over time. Specifically, from 2017 to 2020, the rise in stage 1 cases across age groups was notably more significant compared to 2013 to 2016 and 2009 to 2012. The largest increase occurred in the 50 to 70 age range, with a slower rate of increase in the 30 to 50 age range. Examining the changes in the number of stage 2 lung cancer cases revealed that, as the LDCT scan volume increased over time, so the number of stage 2 lung cancer cases among individuals aged 50 to 70 years gradually increased from 2017 to 2020. Conversely, within the age range of 20 to 50 years, the data indicated relatively stable numbers of stage 2 lung cancer cases over this 3-year period. Analyzing changes in stage 3 lung cancer cases showed a decline among individuals aged 60 to 70 as LDCT scan volume increased from 2017 to 2020. Conversely, within 20 to 60 years, numbers remained relatively stable over the 3-year period. Exploring stage 4 cases, data indicated stability across age groups over the three periods.

Fig. 6figure 6

Exploring the changing distribution of lung cancer cases (stage 0 to stage 4) across different age groups in three distinct time periods (2009–2012, 2013–2016, 2017–2020)

When investigating the changes in the number of stage 0 lung cancer cases across different age groups from 2008 to 2021, stage 0 lung cancer cases were distinctly most prevalent in the age range of 40 to 70 years. However, when looking at the distribution of stage 0 lung cancer cases as a percentage of all diagnosed lung cancer cases, the highest proportion was observed in the 20 to 40-year age group (Fig. 7).

Fig. 7figure 7

Changes in the number and percentage of stage 0 lung cancer in different age groups from 2008 to 2021

Figures 8 and 9 show the fluctuating trends in the impact of LDCT examination volumes on various stages of lung cancer over different time periods, highlighting the corresponding changes in diverse age groups among males. Figure 8 shows the variations in the number of stage 0 lung cancers among males of different ages during the three distinct periods from 2009 to 2020. The volume of LDCT scans clearly increased over time. Stage 0 lung cancers across different age groups exhibited a significantly greater increase in numbers in the period 2017 to 2020 compared with the periods 2013 to 2016 and 2009 to 2012. The age distribution showed a normal increase.

Fig. 8figure 8

Exploring the changing distribution of lung cancer cases (stage 0 to stage 4) across different age groups among men in three distinct time periods (2009–2012, 2013–2016, 2017–2020)

Fig. 9figure 9

Changes in the number and percentage of stage 0 lung cancer among men in different age groups from 2008 to 2021

Next, we examined changes in the number of stage 1 lung cancers among males. A significantly greater increase in the number of stage 1 lung cancers among the different age groups was evident in the period 2017 to 2020 than in the two periods from 2009 to 2016. The group of males aged 50 to 70 years showed the highest increase, whereas the group aged 30 to 50 years displayed a relatively slower rate of increase. In the investigation of stage 2 lung cancers among males, a clear increase over time was noted in the volume of LDCT scans. From 2017 to 2020, the number of stage 2 lung cancers increased gradually among those aged 50 to 70 years. However, among those older than 70 years, a slight decrease in the number of stage 2 lung cancers was observed over this 3-year period.

The exploration of changes in the number of stage 3 lung cancers among males showed a clear increase in the volume of LDCT scans over time. In the period 2017 to 2020, the number of stage 3 lung cancers showed a declining trend among males aged between 60 and 70 years. However, in the 20 to 60-year age group, the number of stage 3 lung cancers remained relatively stable over the 3-year period. Finally, we investigated the changes in the number of stage 4 lung cancers among males: the volume of LDCT scans clearly increased over time. The data showed that from 2017 to 2020, the number of stage 4 lung cancers among males aged 50 to 70 years gradually increased. Conversely, in those older than 70 years, a slight decrease in the number of stage 4 lung cancers was observed during the same period. The number of stage 4 lung cancers among males aged between 20 and 50 years remained relatively stable over the three different years.

We investigated changes in the number of stage 0 lung cancers among males of different age groups from 2008 to 2021. Stage 0 lung cancer was most prevalent in males aged 40 to 70 years. When examining the distribution of stage 0 lung cancer cases as a percentage, the group aged between 40 and 49 years had the highest proportion of stage 0 lung cancer cases among the overall number of diagnosed lung cancer cases (Fig. 9).

The fluctuating trends in the impact of LDCT examination volumes on various stages of lung cancer over different time periods are presented in Figs. 10 and 11, highlighting the corresponding changes in different age groups among females. Figure 10 shows the results of our investigation of the changes in the number of stage 0 lung cancers among females of different age groups during the three periods from 2008 to 2021. The volume of LDCT scans clearly increased over time. From 2017 to 2020, a significantly greater increase in the number of stage 0 lung cancers across different age groups was observed compared with the periods of 2013 to 2016 and 2009 to 2012. The age distribution was normal. Next, we examined changes in the number of stage 1 lung cancers among females. The volume of LDCT scans clearly increased over time: from 2017 to 2020, a significantly greater increase in the number of stage 1 lung cancers among different age groups was observed compared with the other two periods The age distribution showed that the highest increase occurred among females aged between 50 and 70 years, whereas a relatively slower rate of increase occurred among females aged between 30 and 50 years. In our investigation of stage 2 lung cancers among females, compared with the period from 2009 to 2016, a notable increase was evident in the number of stage 2 lung cancers among those aged between 60 and 69 years in the period from 2017 to 2020. However, considering the various age groups from 40 to 70 years, the number of stage 2 lung cancers increased across all age groups as time progressed. Our investigation of changes in stage 3 lung cancers among females showed a decline in cases among those over 60. However, among females aged 30 to 69, numbers remained relatively stable over 3 years. Investigating stage 4 lung cancers among females, data revealed a decrease in cases among those aged 30 to 49 from 2013 to 2020 compared to 2009 to 2012. However, from 2013 to 2020, changes in stage 4 lung cancers across age groups were relatively stable.

Fig. 10figure 10

Exploring the changing distribution of lung cancer cases (stage 0 to stage 4) across different age groups among women in three distinct time periods (2009–2012, 2013–2016, 2017–2020)

Fig. 11figure 11

Changes in the number and percentage of stage 0 lung cancer among women in different age groups from 2008 to 2021

Figure 11 shows the changes in the number of stage 0 lung cancers among females of different age groups from 2008 to 2021. Stage 0 lung cancer was most prevalent in females aged between 40 and 70 years. When examining the distribution of stage 0 lung cancer cases as a percentage of the overall diagnosed lung cancer cases, a significantly higher proportion of stage 0 lung cancer cases was evident among females aged between 20 and 39 years than among those in the other age groups.

Estimated overdiagnosis

We utilized logistic regression to investigate the correlation between individual-level clinical risk factors and stage 0 lung cancer to analyze their impact on potential overdiagnosis. Multivariate logistic regression analysis showed that age, smoking status, and screening status remained significantly associated with stage 0 lung cancer after adjusting for confounding factors (Table 3). Screened status was a strong independent risk factor for stage 0 lung cancer, with an adjusted odds ratio of 7.617 (95% confidence interval, 5.357–10.831; P < 0.001), suggesting a potential overdiagnosis.

Table 3 Logistic regression analysis of clinical parameters for the prediction of patients with stage 0 lung cancer

To further assess the degree of overdiagnosis, we employed a definition of stages 0 to 1 lung cancer. Adoption of this stage 0 to 1 lung cancer definition was based on previous literature reviews and can serve as a broad standard for defining overdiagnosis. However, as we cannot definitively ascertain that all first-stage lung cancers are cases of overdiagnosis at the individual level, using this definition may lead to an overestimation of the extent of overdiagnosis. Furthermore, in the logical analysis, we utilized lung cancer stages 0 to 1 as the outcome events. The multivariate logistic regression analysis indicated that factors such as age, smoking status, female gender, and screening status remained significantly correlated with stage 0 to 1 lung cancer, even after adjusting for confounding factors. Notably, screening status emerged as a robust independent risk factor for stage 0 to 1 lung cancer, with an adjusted odds ratio of 17.114 (95% confidence interval, 11.752–25.011; P < 0.001) shown in Table 4. These findings suggest a more substantial potential for overdiagnosis in the context of stage 0 to 1 lung cancer compared with the context of a definition based solely on stage 0.

Table 4 Logistic regression analysis of clinical parameters for the prediction of patients with stage 0 + 1 lung cancer

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