Inadequate Uptake of USPSTF-Recommended Low Dose CT Lung Cancer Screening

Abstract

In 2023, Journal of Primary Care and Community Health published the results of 4 outstanding studies in which investigators aimed to explore and improve clinician and eligible individuals’ knowledge of the rationale for lung cancer screening (LCS). Their results highlighted the underutilization of LCS, particularly for certain high risk populations, and the continued disparities in screening seen between groups of eligible individuals. Here, key findings from those 2023 Journal of Primary Care and Community Health reports, along with salient findings of other recent LCS reports, are discussed. The bases for the United States Preventive Task Force (USPSTF) LCS recommendations, barriers primary care providers face, the perspective of eligible individuals, importance of shared decision-making (SDM) and disparities between groups in LCS are reviewed along with potential strategies to ensure that more eligible individuals are offered LCS.

Introduction

In the 2022 American Lung Association “State of Lung Cancer” report, the authors noted that the proportion of eligible individuals screened for lung cancer (LC) is “critically low” and Harold Wimmer, National President and Chief Executive Officer of the American Lung Association said “Lung cancer screening is the most immediate opportunity we have to save lives.” ¹ The report stated that 46 states’ Medicaid fee-for-service programs, Medicare and most private payers would cover the USPSTF-recommended low dose CT (LDCT) scanning for the roughly 14.6 million Americans who meet current eligibility criteria for LDCT LCS. Yet more than 10 years since the USPSTF first recommended LCS, screening utilization remains surprisingly low.

Why the USPSTF Recommends Offering LDCT Scanning for Lung Cancer Screening?

Cancer remains the second leading cause of death in the United States. The U.S. health care system has long been criticized for not focusing enough on applying screening tools to improve rates of curing cancers by diagnosing disease earlier. Routine screening recommended by the USPSTF for breast, cervical, and colorectal cancers has resulted in significant decreases in annual mortality as well as mitigating health care costs associated with treating those cancers. ²

Currently, more Americans die of lung cancer (LC) annually than the second (colorectal), third (breast), and fourth (pancreatic) most common causes of cancer deaths combined. As with other cancers, the 5-year survival rate from LC is substantially improved for patients diagnosed with localized disease (56%) compared to distant disease (4.7%). ³ According to the American Cancer Society, 127 070 individuals died of LC in the U.S. in 2023. ⁴ By diagnosing even a small proportion of LCs earlier through screening, many lives would be saved and patients would be spared the adverse effects associated with the newer therapies needed to improve survival for patients with cancers diagnosed at later stages.

In 2011 in “ Reduced Lung-Cancer Mortality with Low-Dose Computed Tomographic Screening” the National Lung Screening Trial Research Team demonstrated that thoracic LDCT screening reduced LC deaths and the rates of death from any cause by 20% and 6.7%, respectively. ⁵ More recently, de Koning et al ⁶ showed that LCS reduced LC mortality with 0.8 less deaths per 1000 person-years. In addition, the Centers for Disease Control and Prevention reported that from 9 studies of LCS the “overall quit [cigarette smoking] rate was 11%” and those who quit reported they were largely motivated to do so by having undergone LCS.^7,8

Before recommending LCS, the USPSTF thoroughly reviewed the published harms and benefits associated with LDCT screening and concluded that “annual screening with LDCT is of moderate benefit for patients at high risk of lung cancer based on age, total cumulative exposure to tobacco smoke and years since quitting smoking.” From 14 studies, the percentage of biopsies done for false positive results ranged from 0.56% to 0.09%. ⁹ Although difficult to accurately estimate, other harms identified included anxiety and distress, radiation exposure complications, and overdiagnoses in small numbers of patients.

In 2013, the USPSTF first recommended that individuals at higher risk for LC should be offered screening with LDCT screening. Currently individuals are eligible for screening-per updated USPSTF guidelines-provided they are age 50 to 80 years, have a 20 pack year cigarette smoking history (eg, 1 pack/day for 20 years) and currently smoke or quit within the last 15 years. ¹ The American Lung Association estimates that screening eligible individuals will reduce the annual death rate from lung cancer by up to 20% ¹ Thus, given the American Lung Association estimate that roughly 127 070 patients die of LC every year and the reduction in mortality predicted by the USPSTF, up to 25 400 lives would be saved each year if all USPSTF-eligible individuals were to undergo LCS.^1,4

Reducing LC mortality by 25 400 individuals would exceed the reductions in mortality estimated by applying the current screening guidelines for any other cancer type. In fact, 25 400 is nearly half the number of patients who die of colorectal cancer and roughly 60% of the number who die of breast cancer annually. ⁴

There is significant variation in estimates of the proportion of eligible patients who undergo screening in part because of the uncertainty in the reliability of the smoking histories of the studied group. Also, LC risk varies between U.S. states likely because the incidence of smoking is different in different states. ¹⁰ Notably, the proportions of eligible individuals screened annually for colorectal cancer and breast cancer are reportedly 71.8% and 67.5%, respectively.^11,12

Based on a survey of USPSTF apparently eligible individuals, Liu et al ¹³ reported that 12.8% underwent LCS. Yet Pham et al ¹⁴ reported that 3 years after the USPSTF first recommended LCS, only 2.0% of eligible individuals were screened and in 2022 the American Lung Association reported that only 4.5% of those eligible for LCS were screened. ¹

Barriers Clinicians Face in Providing LCS

Among the most important ingredients in a recipe to ensure that eligible patients are offered LCS is the need for providers to understand themselves and have time to accurately explain the harms, benefits and uncertainties associated with LCS to appropriate individuals.

From a survey reported in 2021 of 50 providers working in the primary care clinic at Moorhouse University, 78% reported they were aware of the USPSTF guidelines and 54% said they discussed the guidelines with their eligible patients. ¹⁵ Forty-seven percent of the 18% of 1384 primary care providers who responded to a survey in Los Angeles County indicated they were aware of the USPSTF guidelines for LCS screening according to a 2018 report. ¹⁶

From a study of 16 PCCs at Thomas Jefferson and Johns Hopkins Universities, Abubaker-Sharif et al ¹⁷ studied the issue of SDM and found that “many physicians expressed concerns about the time required for SDM and completing SDM about LCS when other issues need to be addressed” but also that physicians participating in their study “would like to receive training in SDM,” that SDM in routine primary care is “challenging but [they] are receptive to additional training in SDM” and that “health systems should take steps to support SDM and LCS performance in primary care.”

Angier et al ¹⁸ recently reported 81 responding primary care clinicians’ understanding of new and updated screening guidelines. They found that 86.4% and 57.8% of male and female clinicians, respectively, recognized that LCS prevented early cancer mortality, and 33.3% of clinicians were unaware of the expanded 2021 USPSTF LCS guidelines.

From Wake Forest School of Medicine, Lewis et al ¹⁹ reported that “few [primary care] providers viewed LDCT as an effective screening modality” and providers cited “patient costs, potential harm from false positive findings, patients’ lack of awareness, risk of incidental findings, and insurance coverage” as barriers to increasing LCS. Also, despite published evidence to the contrary, those investigators found that providers believed that LCS was less effective than breast or colon cancer screening. ²⁰ On the other hand, they found that “guideline knowledge was strongly associated with the use of LDCT.” The authors also noted that “ At least 2 modeling studies have found that the cost per-life saved by LDCT screening compares favorably to cervical, breast, colorectal cancer screening.^19,21,22

Other studies have shown that involving patient navigators can improve LCS. Percac-Lima et al ²³ randomized individuals to receive navigation to confirm eligibility and discuss risk and assure SDM with a formal appointment with a primary care clinician (PCC). When aided with navigation, twice as many patients (ie, 92%) underwent LDCT scanning, compared to screening uptake using an approach without navigation. In the Lahey Clinic LCS program, which also involved navigation to retain individuals, adherence to LCS in their screened cohort was >80%. ²⁴

Other investigators have attempted to improve LCS screening by focusing on those among the eligible high risk group most likely to benefit from screening. For example, PCCs might focus on giving more attention and SDM time to those eligible who also have strong family histories or apparent pathogenic variants that predispose to LC rather than with elderly individuals, for example, whose comorbidities might represent a contraindication to intervention, should LC be discovered.^25,26

In the Lynchburg Virginia area, a Nurse Practitioner (NP)-based Lung Cancer Screening Program was established in 2015 with the recognitions that “inherent to NP practice is the concept of guidance and coaching on many levels, including a holistic approach to health promotion” and that NPs are “uniquely positioned to guide patients through lung cancer screening” because they often have more training and experience in the complicated reimbursement issues that might be challenges for other providers. ²⁷

In an ambitious project, Lin et al ²⁸ used a “theory-informed approach” to identify 15 common factors (9 barriers and 6 facilitators) that affected LCS in 34 relevant studies and combined these factors to tailor LCS recommendations or interventions. Others have suggested that combining risk factors with emerging biomarkers that predict LC (eg, detectable ctDNA) could be used to identify those individuals most likely to benefit from LCS. ²⁹

How Individuals View Lung Cancer Screening?

Studies suggest that a significant proportion of individuals favor being offered LCS. For example, in 2016, the UK Lung Cancer Screening Trial published results showed that among individuals with an estimated risk of greater than 5%, 30.7% of those surveyed “responded positively to the [LDCT] screening invitation.” The investigators also concluded that the individuals randomized to receive LDCT scanning experienced only modest and temporary short term psychosocial issues and their health economic analysis suggested that LDCT screening could be cost effective. ³⁰

Ziller et al ³¹ reported on six patient focus groups surveyed in rural Maine. Although participants recognized their elevated LC risk, “few were aware of LDCT screening. When informed about LDCT, most participants indicated a willingness to undergo screening, although a substantial minority indicated reluctance related to fear and fatalism” and patients identified attention and time for listening to their concerns, “respect and non-judgmental, non-stigmatizing attitudes; treating patients as individuals; and provider empathy and emotional support” as qualities they valued in their providers.

Beginning with the 2013 USPSTF recommendation for LCS for individuals at higher risk, other articles have confirmed individuals interest in LCS. For example, from a 2011 telephone survey of 1290 former and current smokers, Delmerico et al ³² reported that 78.5% and 81.4% of current and former smokers, respectively, were willing to undergo LCS if it was recommended by their physician. Also, lack of insurance coverage and fear of finding out they have cancer were the most common barriers to willingness to be screened. In 2023 Behr reported that among over 1400 former smokers surveyed, 70.3% were willing to undergo screening for LC and COPD. ³³

Quaife et al ³⁴ offered ever-smokers a lung health check and follow-up questionnaire explaining the risks and benefits of LCS to individuals. LCS was increased for individuals who developed both positive and negative perceptions of LCS from their participation on the study. The authors concluded that “changing perceptions” might increase LCS, particularly for those at high risk.

A feasibility study evaluated an online tool for individuals of a large primary care practice who were eligible for LCS per the USPSTF criteria. Those individuals who used the tool were more likely to undergo LDCT scan screening. The authors concluded “This non-persuasive high-quality shared decision-making intervention significantly increased lung cancer screening and was feasible in real-world clinical care.” ³⁵

In another study, 229 participants were randomly assigned to view an information film about the harms and benefits of LCS and receive an information booklet or instead receive only the booklet. The group who both watched the film and was given the booklet showed the greatest improvement in their knowledge score (P = .007 in the multivariant analysis) and, for those who reviewed both the film and the booklet, decisional certainty was improved compared to those only receiving the booklet. ³⁶

What affects patient interest and disparities between groups in what affects their interest in LCS is key to planning effective treatment programs. For example, reports have consistently demonstrated concerns related to there being a stigma associated with having a LC diagnosis, inaccurate LC-risk perception, concerns about exposure from LDCT radiation, and the misperception that diagnosing LC prior to experiencing symptoms offers no advantage are common reasons for individuals declining LDCT scanning.^{34 -39}

From a survey conducted in Indiana, the investigators found white participants more likely intended to partake in LCS compared to Black participants. Also, participants in urban areas were much more likely unaware of LCS options ( 64.5%) than were those living in suburban (10.2%) and rural (25.3%) areas. ⁴⁰

Shared Decision-Making

SDM discussions are mandated for coverage of LCS by the Centers for Medicare and Medicaid Services (CMS). ⁴¹ SDM involves a collaborative process between the individual and health-care providers that allows for patients eligible for LCS to make truly informed decisions about whether to proceed with LCS after carefully weighing the harms and benefits of LCS.

Appreciating their individualized risk is critical for SDM. Rutten et al ⁴² showed that among respondents to a survey those with some college (OR = 1.76) and college degrees (OR = 2.13) more accurately estimated their LC risk than those with less than a high school education. Also former smokers (OR = 2.53) more accurately reported their LC risk than current smokers. Clearly, clinicians must first help all patients appreciate their LC risk.

SDM might sometimes involve disabusing individuals of what has been referred to as fatalistic beliefs about cancer which might influence an individual’s interest in screening. Niederdeppe and Levy ⁴³ surveyed individuals and found that 71.5% agreed “ There are so many recommendations about preventing cancer, it’s hard to know which ones to follow.” Although LCS is encouraged for early detection, with this sizable majority agreeing that advice for prevention is not valuable, it might be reasonable to conclude they would feel similarly about early-detection advice.

Considering the particular goals, values, and preferences of every individual who is considering LCS is also key in advising individuals about whether to pursue LCS. Therefore, a SDM discussion, during which the provider thoroughly explains the harms, benefits, and uncertainties of LCS is critical before a screening program is initiated.

Barriers to effective LCS SDM include lack of presenting a clear and accurate, balanced and thorough discussion of the harms and benefits of LCS. There is evidence that some eligible Individuals do not adequately understand the information presented to them, and some patients and providers prefer to not have SDM discussions. ³⁹

SDM tools have been applied to help individuals with LCS SDM. Walsh et al ³⁷ showed that individuals who used a computer tablet-based tool called LungCARE while in the waiting room of their primary care provider’s clinic were more likely to discuss LCS with their providers (56 vs 25%; P = .04) and were more likely to complete a LCS program (32% vs 13%; P < .01), and had statistically significantly higher knowledge scores after using the tool than those patients not using LungCARE. The authors concluded that applying their tool will improve the LCS SDM.

Also, investigators have recognized that barriers to SDM and LCS might differ in different populations. For example, Robichaux et al ⁴⁴ assessed uptake of LCS in an urban Native American clinic by providing individuals either a single culturally-targeted mailer or the same mailer plus a follow-up text message and additional mailing. The investigators proposed that SDM discussions need to be personalized according to their patients notions about not just the harms, but the perceived benefits of tobacco. The investigators felt that SDM would represent “an opportunity to explain the benefits of reclaiming traditional tobacco and honoring bodily autonomy through appropriate cancer screening” as well as ensuring that other important harms and benefits of LCS would be provided this group of individuals because providers at the clinic in the study were trained in SDM, indications for LCS, and the process for referral to a LCS center. Unfortunately, with either strategy, very few patients scheduled a SDM visit (ie, 8.5%) and the authors concluded that further efforts were needed to “resolve barriers to lung cancer screening” and “to ensure this group is equitably engaged in shared decision-making regarding lung cancer screening.”

McDonnell et al ⁴⁵ also recognized that NPs have a key role in discussing LCS with individuals. The investigators developed a 32-item questionnaire and a semi-structured telephone interview. They concluded that NPs believe “shared decision making [SDM] with their high risk patients about LDCT is within their scope of practice” but that NPS have “limited abilities to improve the uptake of LDCT” and that “disseminating guidelines and authorizing health insurance reimbursement is insufficient.”

Mitigating Disparities in LCS

Disparities exist between groups for which individuals undergo LCS. Japuntich et al ⁴⁶ showed that non-Black individuals were 2.8 times more likely to receive LDCT scanning than eligible Black patients. Richmond et al ⁴⁷ demonstrated that Black individuals in North Carolina “ may be less likely than White individuals to receive LDCT screening” based on a retrospective chi-squared test to assess potential racial disparities.” Based on simulation modelling, which includes factoring the higher incidence of smoking among Black persons, Barry et al ⁴⁸ estimated that the 2021 USPSTF-updated LCS recommendations, which expanded the criteria for eligible individuals for LCS, would increase screening relatively by 78% in non-Hispanic White persons, 107% in non-Hispanic Black persons, and 112% in Hispanic/Latino persons.

In their survey, Carter-Harris et al ⁴⁰ demonstrated that respondents living in rural area had the statistically significant highest total knowledge scores related to their lung cancer risks and even after adjusting for sociodemographic variables. ⁴⁰ Their results underscore the need to improve education for particular groups, as an important step toward LCS.

From a study in rural Alabama, Copeland et al ⁴⁹ found that although physicians were influential in continuing LCS programs, physicians were “not very influential in decisions to initiate screening.” Screening more likely resulted from information provided by Community Health Advisors (CHAs), friends, or others. They concluded that “Future research is warranted to further explore use of CHAs in lung cancer screening” and also that, for rural, predominantly Black communities in Alabama “having multiple messengers and educational advertising can support increased awareness and interest in lung cancer screening.” Their results suggest that uptake is impacted by who is participating in the SDM discussions.

In their thorough review of disparities in LCS, Haddad et al ⁵⁰ noted that in areas where there is a higher incidence of LC, there are actually less nearby screening facilities, and Black smokers have lower LCS rates compared to white smokers. The authors concluded that “ Implementation of lung cancer screening and smoking cessation programs requires addressing community beliefs regarding . .the risk of lung cancer, a risk that is not well understood among individuals with low socioeconomic status. ⁵⁰

Furthermore the authors concluded that “a generational history of discrimination and mistrust contributes to perceptions of stigma and challenges with patient-provider communication” and they suggested that effective LCS programs must also address community perceptions of LC risk, something not well understood in individuals of low socioeconomic status. ⁵⁰

Conclusions

Published evidence suggests that a significant proportion of eligible patients wish to undergo LCS and that patients and clinicians are interested in and need more education related to the potential harms, benefits, and uncertainties of LCS to ensure efficient and effective SDM discussions. Hopefully, with an improved understanding of the clinical utility of LCS, busy PCCs and others responsible for SDM discussions will have time to offer LCS to all appropriate patients who can then make truly informed and personalized decisions about whether to pursue LCS.