A narrative review of lung cancer screening: from adoption to maturity

Introduction

Background

Lung cancer is the leading cause of cancer-related deaths both worldwide and in the United States (1). Currently, eligibility for lung cancer screening includes individuals aged 50–80 with a history of tobacco use of at least 20 pack-years, and current smokers/those who have quit smoking within the past 15 years. Low-dose computerized tomography (LDCT) scan of the chest is the current lung cancer screening modality and have been shown to reduce lung cancer mortality by 20% compared to chest radiography (2). Despite this benefit, only 6% of eligible patients participate in lung cancer screening (3). Opportunistic lung cancer screening could offer potential advantages, though its impact on long-term survival remains unclear.

Rationale and knowledge gap

Opportunistic lung cancer screening is not well understood and there is limited data on its impact on lung cancer-related mortality.

Objective

Our literature review aims to examine current lung cancer screening practices, their effect on surgical decisions, and its role in opportunistic screening. We present this article in accordance with the Narrative Review reporting checklist (available at https://asj.amegroups.com/article/view/10.21037/asj-24-40/rc).

Methods

For our review, we utilized PubMed as our search engine. An initial search was conducted using the keywords “lung cancer screening”, “low dose CT”, and “early detection”. An exclusion filter for the keywords “non-lung cancers”, “general cancer treatment” and unrelated screening methods” was subsequently utilized to narrow our search pool to key relevant terms. To allow for a refined, more focused search, we integrated more relevant concepts to our search: “lung cancer screening implementation”, “LDCT in healthcare”, and “screening policies”. Our final keyword set for review comprised of the following: “lung cancer screening”, “LDCT early detection”, and “healthcare system policies for screening”. All years were considered. In the end, 36 studies were included for our review. Our rigorous methodology allowed for transparency in our review and maximized the validity of our research. Table 1 summarizes our search strategy summary.

The value of lung cancer screening

Lung cancer screening programs have a history dating back to the early 1980s, particularly at the Mayo Clinic’s Mayo Lung Project. The Mayo Lung Project conducted a double-arm randomized screening study to evaluate the effectiveness of periodic screenings in reducing lung cancer mortality rates (4). The study involved 9,211 male smokers, with half of them randomly assigned to the intervention arm. The intervention group underwent chest radiographs and sputum cytology every four months for six years. The control arm group, on the other hand, received annual chest radiographs. The results showed that the lung cancer mortality rate in the intervention arm was 4.4 deaths per 1,000 person-years [95% confidence interval (CI): 3.9–4.9]. In contrast, the mortality rate in the usual-care arm was 3.9 deaths per 1,000 person-years (95% CI: 3.5–4.4). Despite these differences, the study found no significant mortality benefit in chest radiographs screening (P=0.09).

Notably, the impact of lung cancer screenings with modern chest radiographs on mortality rates was examined in the prostate, lung, colorectal, and ovarian (PLCO) randomized trial (5). Over 150,000 patients were randomly assigned to either annual screening with anterior-posterior chest radiographs or no imaging. During a 13-year follow-up period, the study revealed a lung cancer incidence rate of 20.1 per 10,000 person-years in the intervention group and 19.2 per 10,000 person-years in the usual care group [relative risk (RR) 1.05, 95% CI: 0.98–1.12]. Consequently, a total of 1,213 lung cancer deaths were observed in the intervention group, resulting in a mortality rate of 14.0 per 10,000 person-years. Similarly, 1,230 lung cancer deaths were recorded in the usual care group, leading to a mortality rate of 14.2 per 10,000 person-years. Unfortunately, this study also demonstrated no mortality benefit with chest radiograph screening, as evidenced by a RR of 0.99 (adjusted 95% CI: 0.87–1.22; adjusted P=0.48).

The addition of lung cancer screening via LDCT modality was pivotal in establishing survival benefit in comparison to chest radiographs. In the National Lung Screening Trial (NLST) (2), a multicenter randomized control trial, nearly 54,000 high-risk individuals were enrolled and randomly assigned to undergo either three annual screenings with LDCT or a single anterior-posterior chest radiograph. During all three screening rounds, the LDCT group had a statistically higher rate of positive screening results compared to the chest radiograph group. At T0 (time of screening), the positive screening rate was 27.3% in the LDCT group vs. 9.2% in the chest radiograph group. This rate increased to 27.9% at T1 and 16.8% at T2. A total of 1,060 lung cancers were diagnosed in the LDCT group compared to 941 lung cancers diagnosed in the chest radiograph group. The RR of lung cancer diagnosis in the LDCT group was 1.13 (95% CI: 1.03 to 1.23). In the LDCT group, 649 cancers were diagnosed after a positive screening test, while 44 cancers were diagnosed after a negative screening. The remaining 367 patients either missed their screening or received the diagnosis after the trial ended. In the chest radiograph group, 279 cancers were diagnosed after a positive screening test, 137 after a negative screening test, and the remaining 525 patients either missed their screening or received the diagnosis after the trial ended. The mortality rate in the LDCT group was 0.25% (n=144,103) and 0.31% in the chest radiograph arm (n=143,368). This resulted in a relative reduction in lung cancer mortality with LDCT screening of 20% (95% CI: 6.8% to 26.7%; P=0.004). Therefore, LDCT screening demonstrated a mortality benefit. This benefit with LDCT screening was ascertained during the Nederlands–Leuvens Longkanker Screenings Onderzoek (NELSON) trial (5). In this randomized control trial, patients who underwent LDCT screening had a significantly improved survival rate compared to those who did not. At the 10-year follow-up, the lung cancer mortality rate in the screening and control groups was 2.50 and 3.30 per 100 person-years, respectively. The cumulative RR for death from lung cancer in the screening group was 0.76 (95% CI: 0.61 to 0.94; P=0.01) (6).

Despite the advantages of lung cancer screening, its limitations have been extensively studied. According to existing literature (2,7), false positives following LDCT screenings have ranged from 7.9% to 96%. These false positive findings can lead to invasive and potentially harmful subsequent diagnostic procedures. Follow-up diagnostic interventions, such as CT-guided or navigational lung biopsy (8), mediastinoscopy, or surgical lung biopsy (9-13), have morbidity rates ranging from 0.08% to 19%. These resulting interventions may result in overtreatment of benign lesions. In the NLST, 23% of the surgical procedures performed for a positive screen were performed on benign lesions. Furthermore, 0.06% of the false positive results resulted in an adverse event after an invasive diagnostic procedure. The U.S. Preventive Services Task Force (USPSTF) thus concluded that these benefits are justified in the highest-risk patients (14).

Adherence: the Achilles heel of lung cancer screening

In 2022, lung cancer screening adherence rose to 16%, up from 12% in 2019. However, it remains significantly low when compared to other disease sites’ cancer screening track records, such as breast (64%), cervical (75%), colorectal (59%), and prostate (35%) (15,16). Several factors contribute to the low adherence to lung cancer screening. The low adherence to lung cancer screening is due to various attitudinal and systematic barriers, including its eligibility focus on age and tobacco. Factors like social stigma, increased public education, and socioeconomic status have reduced tobacco use, yet smokers from disadvantaged backgrounds face low screening rates due to limited access to healthcare and insurance. More than 50% of eligible current and former tobacco users lacked insurance or were on Medicaid, restricting their financial ability to get screened or treated (17,18).

Stigma has been identified as a substantial barrier to lung cancer screening. A qualitative study at Indiana University involving 26 patients revealed that stigma, particularly “self-blame” or “guilt” over tobacco use, discourages many smokers from participating in lung cancer screening (19). This stigma often leads to delayed screening and can cause self-reporting bias during clinician assessments of tobacco use, potentially resulting in missed screening opportunities. Additionally, a UK study found higher cancer-related stigma in men and minorities, which correlates with lower participation in lung cancer screening (20). The issue is further compounded by insufficient electronic medical record (EMR) notifications. This is primarily due to inaccurate tobacco documentation and uncertainty about patient eligibility (21).

Inadequate education for physicians and advanced practitioners may exacerbate these challenges (22). In 2019, 75% of providers acknowledged the benefits of lung cancer screening over its risks, but only 50% believed in its survival benefits. Many were also unaware of Medicare and Medicaid insurance coverage for lung cancer screening. A 2022 prospective study demonstrated the positive impact of an educational series for physicians. After introducing the series, the percentage of eligible patients undergoing lung cancer screening increased from 27% to 62%, indicating a significant effect (P<0.0001) (23).

Opportunistic lung cancer screening: a window of opportunity

Lung cancer, the leading cause of cancer-related mortality in women, presents a significant disparity in adherence rates between lung cancer screening and breast cancer screening. This gap presents an opportunity to enhance lung cancer screening. Notably, lung cancer mortality rates for women (25.9%) surpass the combined remaining cancer-related deaths in women (breast, ovarian, and cervical cancer) (18.7%, 5.7%, and 0.7%, respectively) (24-27). The role of concomitant screening has been explored in limited centers. Opportunistic lung cancer screening involves screening outside a regimented program and capitalizing on screening opportunities during medical encounters. In Yue et al.’s prospective survey study, patients who were eligible for mammogram screening were dually screened for lung cancer screening eligibility and offered enrollment in their pilot dual screening program (28). Results from the survey demonstrated 54 patients (98%) felt they were at risk for lung cancer and 80% expressed motivation for early detection screening. However, significant barriers were involved: 58% lacked knowledge regarding lung cancer screening eligibility and 47% reported concerns related to costs. This highlights the fact that dual breast cancer and lung cancer screening is a feasible intervention that could aid in early detection of lung cancer and potentially improve mortality rates. Remarkably, Sandler et al. demonstrated a correlation between women undergoing breast cancer screening and lung malignancy-related mortality rates (29). In their study, 251 women undergoing screening mammography were simultaneously eligible or met the criteria for lung cancer screening under the USPSTF guidelines. Four years after the study’s initiation, 63 of the eligible women (25%) had enrolled in lung cancer screening. Notably, 16 (6.37%) new cancer diagnoses were reported among the dual screening-eligible women, with 4 (1.59%) being breast cancer diagnoses and 10 (3.98%) being lung cancer diagnoses. There were five lung cancer-related deaths (50%), all of which occurred in the sub-population of patients who were not enrolled in lung cancer screening. In contrast, there were no deaths among women who had screening-detected lung cancers. There were no deaths from breast cancer.

There are several factors to consider when combining cancer screenings. From a technical standpoint, there may be a long delay between interpreting simultaneous cancer imaging or a limited number of radiologists who can interpret both imaging modalities. Additionally, the stigma and phobias associated with radiation may impact patient participation. Additionally, the findings on the benefits of concurrent breast cancer and lung cancer screenings are not consistent across all types of cancers. For example, Mascalchi et al. (30) assessed the feasibility of concurrent lung cancer screenings using LDCT and colon cancer screenings using CT colonography. Currently, colon cancer and lung cancer screenings have distinct recommended screening frequencies. The USPSTF recommends CT colonography every five years for an average-risk individual, which means that changing the frequency of either screening could lead to missed lung cancers (if decreasing LDCT frequency) or increased radiation exposure, incidental findings, and invasive procedures (if increasing CT colonography frequency). This rate-limiting step poses a challenge for combining the two screenings.

Throughout the literature, opportunistic lung cancer screening appears to provide mortality benefits. Wang et al.’s 2023 study in mainland China evaluated the prognostic impact of opportunistic screening with LDCT (31). In China, the guideline recommends LDCT screening for individuals aged 50–74 years who are heavy smokers, exposed to passive smoking, have chronic obstructive pulmonary disease (COPD), a history of occupational exposure, or a family history of lung cancer (32). While guideline-driven LDCT screening has been shown to reduce lung cancer mortality, socioeconomic and cost barriers hinder participation and subsequent benefits. This cohort study included 5,234 patients with lung cancer. Of these, 2,251 (42.9%) received their lung cancer diagnosis through opportunistic screening, while the remaining 2,983 (57.1%) were diagnosed based on symptoms prompting further workup. Kaplan-Meier estimates revealed a higher survival rate in the opportunistic screening group compared to the non-opportunistic group (χ²=830.8; P<0.001). Furthermore, univariate Cox regression analysis demonstrated a lower lung cancer incidence (34%, hazard ratio of 0.66; 95% CI: 0.55–0.80) and all-cause mortality risk (18%, hazard ratio of 0.69; 95% CI: 0.58–0.83) associated with opportunistic screening.

Furthermore, despite the known association between lung cancer and cardiovascular disease (CVD), the advantages of lung cancer screening in patients with CVD remain unclear. Patients with lung cancer have a significantly increased risk of CVD, with a 66% higher risk of developing CVD and an 89% higher risk of coronary artery disease alone (33,34). Several modifiable risk factors and subsequent pathophysiological mechanisms contribute to the increased risk of both cancer and CVD. Handy et al. discussed the feasibility of coronary artery calcium (CAC) quantification (a marker for CVD) in conjunction with concurrent lung cancer screening (35). However, only approximately 40% of the lung parenchyma is reconstructed during cardiac CT performed for CAC assessment. Consequently, less than 1% of cardiac CT detects lung cancer (36,37).

Correlating lung cancer screening with post-surgical outcomes

Kamel’s group described the outcomes of surgical intervention in patients following the NLST protocols (38). Among the 53,454 enrolled patients, 4.8% underwent one or more invasive procedures. The most common procedures were lobectomy (80%), pneumonectomy (4.1%), and sublobar resection (16.1%). The post-operative morbidity rate was 30.8%, with 15.5% considered major complications (95% CI: 13–18%). Notably, the overall 30-day mortality rate was only 1.7% (P=1). After conducting a multivariable analysis, prolonged smoking pack history and pulmonary comorbidities were strongly associated with increased morbidity and mortality. Patients who underwent sublobar resection (odds ratio, 0.59; 95% CI: 0.38–0.94) or Video-assisted thoracoscopic surgery (VATS) (odds ratio, 0.76; 95% CI: 0.56–1.04) experienced fewer complications and deaths compared to those who underwent lobectomy. In line with the “Patient and Physician Guide: National Lung Screening Trial (NLST)” from the National Cancer Institute, there is a clear benefit in mortality reduction for patients who undergo LDCT screening (39). However, it is essential to consider the risks associated with false positive detection and diagnostic interventions for benign disease. The potential benefits of LDCT may also influence surgical outcomes. Okusanya’s group analyzed data from the National Cancer Database (NCDB) and included 1,003 patients from the NLST in their study. The NCDB hospitals were found to have statistically significantly higher mean 30-day and 90-day mortality rates compared to the NLST hospitals. The mean 30-day mortality rate in the NCDB hospitals was 2.2 (95% CI: 2.2 to 2.2) vs. 1.8 (95% CI: 1.8 to 1.8) in the NLST hospitals, with a p-value less than 0.001. Similarly, the mean 90-day mortality rate in the NCDB hospitals was 4.2 (95% CI: 4.2 to 4.3) vs. 2.9 (95% CI: 2.9 to 2.9) in the NLST hospitals, with another p-value less than 0.001 (40). These findings highlight a discrepancy between current practice patterns and the NLST recommendations. Further studies are necessary to determine the impact of lung cancer screening on surgical outcomes in patients who undergo resection.

Financial implications of lung cancer screening

LDCT can add $1.3–2 billion to annual national healthcare expenditures (41). In the 2022 “State of the Lung” by the American Lung Association, of the 14.2 million Americans meeting guidelines for screening, only 5.8% had been screened with rates as low as 1% in some states (42). Of the numerous reasons for this discord in screening rates, health literacy, health disparities, etc., the financial implications remain the most impactful to the population. Fee-for-service Medicaid programs are not required to cover lung cancer screenings for high-risk populations. Per the American Lung Association, 46 states’ Medicaid provides coverage for LDCT screening, and subsequent testing and procedures may be costly, which adds another barrier to lung cancer screening.

While early screening interventions mitigate the health burdens of lung cancer, it is equally important to be cognizant of the economic burden in contrast to the cost of treatment for advanced lung cancer. Using the Surveillance, Epidemiology, and End Results (SEER)-Medicare database for years 1998–2013, Sheehan et al. sought to assess the lung cancer treatment cost over the course of the phase of care (43). SEER compiles the clinical, demographic and cause of death information across 17 cancer registries in the United States, which is estimated to represent 28% of the US population. The SEER-Medicare links the data for people diagnosed with cancer in the SEER region and is enrolled in Medicare. A total of 145,988 people were included in the analysis. In patients in the continuing phase, which had a median length of 21.8 months, the average monthly attributable cost ranged from $1,269 (95% CI: $1,049 to $1,490) (stage IV non-small cell lung cancer (NSCLC) patients receiving supportive care) to $5,756 (95% CI: $4,937 to $6,574) (stage III NSCLC patients who were receiving chemotherapy). In the terminal phase, defined as the 6 months preceding the patient’s death, the average monthly cost ranged from $13,426 (95% CI: $13,242 to $13,610) vs. $13,840 (95% CI: $13,471 to $14,208). Hence, LDCT not only benefits the patient, but it may lessen the high financial burden associated with management of advanced lung cancer.

Limitations

This review of lung cancer screening studies faces several limitations. First, the data predominantly relies on existing studies, which vary in methodologies and sample populations. This heterogeneity makes it challenging to draw standardized conclusions across different screening programs and populations. Additionally, there is a lack of comprehensive studies that address the time intervals from positive screening to biopsy, surgery, and subsequent surveillance imaging, limiting our understanding of the full continuum of lung cancer care. The review also does not capture data on the diagnosis rates of advanced disease at screening, as advanced stages are typically identified clinically rather than through screening programs. Furthermore, while opportunistic lung cancer screening appears promising, the number of studies exploring its impact is minimal, underlining the need for more research to validate its feasibility and effectiveness. Lastly, biases related to patient adherence, socioeconomic factors, and geographic differences in screening access are not fully accounted for, potentially affecting the generalizability of findings.

Conclusions

Lung cancer screening with LDCT has shown significant survival benefits for eligible patients. However, adherence remains low compared to other cancer screenings due to barriers like stigma, socioeconomic challenges, and limited awareness. Opportunistic screening offers potential to bridge these gaps, but further investigation is needed to assess its feasibility, cost-effectiveness, and long-term outcomes. Critical questions also persist about optimizing screening frequency, integrating with other screening modalities, and managing false positives.

Future research should focus on reducing disparities in access and adherence, particularly for underserved populations, and exploring the impact of enhanced education for both patients and healthcare providers. By addressing these challenges, screening rates could improve, reducing lung cancer mortality. Ultimately, a more integrated approach combining structured and opportunistic strategies may provide the most effective pathway for early detection and better patient outcomes.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://asj.amegroups.com/article/view/10.21037/asj-24-40/rc

Peer Review File: Available at https://asj.amegroups.com/article/view/10.21037/asj-24-40/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://asj.amegroups.com/article/view/10.21037/asj-24-40/coif). R.B. received funding from the Thoracic Surgery Foundation through a resident research grant to develop a lung cancer screening tool unrelated to this manuscript. D.O. received funding from the Agency for Healthcare Research and Quality (AHRQ) (No. R01HS02934301A1) and he is the Fry meeting Professor at the University of Chicago. C.N.E. received speaker honoraria from AtriCure and consultation fees from Johnson & Johnson MedTech, and Cook Medical. The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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