Abstract
Introduction:
We aimed to calculate percent up-to-date with testing in the context of lung cancer screening (LCS) across five healthcare systems and evaluate differences according to patient and health system characteristics.
Methods:
LCS-eligible individuals receiving care within the five systems in the Population-based Research to Optimize the Screening Process Lung consortium (PROSPR-Lung) from 10/1/2018 – 9/30/2019 were included in analyses. Data collection was complete 6/15/2021; final analyses were complete 4/1/2022. Chest CTs and patient characteristics were obtained via electronic health records and used to calculate percent completing chest CT in the prior 12 months (considered up-to-date). The association of patient and healthcare system factors with being up-to-date was evaluated with adjusted prevalence ratios (PRs) and 95% CIs using log-binomial regression models.
Results:
There were 29,417 individuals eligible for LCS as of 9/30/2019; 8,333 (28.3%) were up-to-date with testing. Those ages 65–74 years (PR = 1.19; CI: 1.15–1.24, vs. ages 55–64), with COPD (PR = 2.05; CI: 1.98–2.13), and in higher SES census tracts (PR = 1.22; CI: 1.16–1.30, highest quintile vs. lowest) were more likely to be up-to-date. Currently smoking (PR = 0.91; CI: 0.88–0.95), having a BMI ≥ 30 kg/m2 (PR = 0.83; CI: 0.77–0.88), identifying as Native Hawaiian or Other Pacific Islander (PR=0.79; CI: 0.68–0.92), and having a decentralized LCS program (PR = 0.77; CI: 0.74–0.80) were inversely associated with being up-to-date.
Conclusions:
Percent up-to-date with testing among those eligible for LCS is well below up-to-date estimates for other types of cancer screening and disparities in LCS participation remain.
Keywords: Equity, Lung Cancer Screening, Quality
Introduction
From 2013 through 2020, the US Preventive Services Task Force (USPSTF) recommended annual lung cancer screening (LCS) via low-dose computed tomography (LDCT) for 55- to 80-year-olds with 30+ pack-years smoking history who currently smoke or quit within the last 15 years.1 In 2021, guidelines expanded to include 50- to 80-year-olds with 20+ pack-years.2 Although there are currently no nationally-adopted quality metrics for LCS, the National Committee for Quality Assurance Healthcare Effectiveness Data and Information Set (HEDIS) metrics for cancer screening in breast, colorectal, and cervical cancers are based on percent of the screening eligible population that is up-to-date with a test that can be used for cancer screening.3 By evaluating differences in percent up-to-date according to patient- and system-level factors, healthcare systems can better understand and address equity in LCS.
Methods
Study participants were patients ages 55–80 years who received care within healthcare systems in the Population-based Research to Optimize the Screening Process Lung Consortium (PROSPR-Lung) from 10/1/2018 through 9/30/2019. PROSPR-Lung is a collaboration of 5 healthcare systems, including: Henry Ford Health (HFH), Kaiser Permanente Colorado (KPCO), Kaiser Permanente Hawaii (KPHI), Marshfield Clinic Health System (MCHS), and the University of Pennsylvania Health System (UPHS), as previously described.4
Data on chest CTs and patient characteristics were obtained via electronic health records (EHR). Data from EHRs were used to apply the USPSTF 2013 criteria to identify individuals who were alive and eligible for LCS as of 9/30/2019. Smoking history was from standard fields within the EHR that can be updated at any encounter; information from the encounter most proximal, but prior to or on, 9/30/2019, was use. Chest CT procedure codes (S8032, G0297, 71250, 71260) were used to identify chest CTs.
Consistent with the measurement of “up-to-date” with testing used as a HEDIS metric for cancer screening of other organ sites with a USPSTF grade A or B recommendation,5 those receiving a chest CT regardless of indication in the 12 months prior to 9/30/2019 were considered “up-to-date” with testing. Exclusions included individuals with: 1) lung cancer prior to 10/1/2018; 2) missing smoking data needed to ascertain LCS eligibility; 3) a 90-day gap in health plan membership from 10/1/2018–9/30/2019 in membership-based systems (HFH Health Alliance Plan, KPCO, KPHI, and MCHS); and 4) without a primary care visit during the 3 years prior to 9/30/2019 at non-membership-based systems (HFH and UPHS).
The Yost Index, a composite measure of SES, was based on census tract of residence.6 Individuals were classified as belonging to a healthcare system with a centralized or decentralized LCS program using information from key informants, as previously described.7 Centralized programs used core staff and centralized processes, tracking, or outreach for LCS; whereas decentralized programs relied on primary care or specialist providers to engage patients in LCS. During the analysis time period, 3 health systems’ LCS programs were centralized and 2 were decentralized.
The association of patient (age, sex, race, ethnicity, and Yost Index, smoking status, BMI, and chronic obstructive pulmonary disease (COPD)), and healthcare system factors (decentralized vs. centralized LCS program) with being up-to-date with testing was evaluated with marginal prevalence ratios (PRs) and 95% CIs using log-binomial regression models with a robust sandwich estimator. Unadjusted PRs and PRs adjusted for each factor specified above were estimated. Study protocols were approved with a waiver of consent due to use of only retrospective EHR data (approval number: CO-17–2466) by the KPCO IRB.
Results
Among those ages 55–80, 71% had complete smoking data to ascertain LCS eligibility. Of these, 29,417 met USPSTF 2013 criteria as of 9/30/2019 and 55% were men, 87% ages 55–74 years old, 53% formerly smoked, 30% had COPD, and 67% were in a health system with centralized LCS. The racial and ethnic distribution was: 73% White, 14% Black, 3% Hispanic, 3% Asian, and 2% Hawaiian or Other Pacific Islander (Table 1).
Table 1.
Characteristics of the PROSPR-Lung cohort eligiblea for lung cancer screening as of September 30, 2019.
| Characteristic | N | % |
|---|---|---|
| Total | 29,417 | |
| Age (years) | ||
| 55 – 64 | 13,125 | 44.6 |
| 65 – 74 | 12,414 | 42.2 |
| 75 – 80 | 3,878 | 13.2 |
| Sex | ||
| Male | 16,020 | 54.5 |
| Female | 13,397 | 45.5 |
| Race or Ethnicity | ||
| Hispanic | 922 | 3.1 |
| Non-Hispanic Asian | 848 | 2.9 |
| Non-Hispanic Black | 4,152 | 14.1 |
| Non-Hispanic Hawaiian or Other Pacific Islander |
538 |
1.8 |
| Non- Hispanic White | 21,361 | 72.6 |
| Unknown or Another Race | 1,596 | 5.4 |
| Smoking Status | ||
| Current | 13,842 | 47.1 |
| Former | 15,575 | 52.9 |
| Type of LCS Program | ||
| Centralized | 19,822 | 67.4 |
| Decentralized | 9,595 | 32.6 |
| Health System | ||
| Henry Ford | 11,502 | 39.1 |
| Kaiser Permanente Colorado | 6,311 | 21.5 |
| Kaiser Permanente Hawaii | 2,009 | 6.8 |
| Marshfield Clinics | 2,581 | 8.8 |
| University of Pennsylvania | 7,014 | 23.8 |
| Chronic Obstructive Pulmonary Disease | ||
| No | 20,739 | 70.5 |
| Yes | 8,678 | 29.5 |
| Body Mass Index (kg/m2) | ||
| < 25 | 8,562 | 29.1 |
| 25 – 29 | 9,681 | 32.9 |
| 30 + | 11,040 | 37.5 |
| Missing | 134 | 0.5 |
| Yost Index Quintile | ||
| Quintile 1 (lowest) | 6,332 | 21.5 |
| Quintile 2 | 5,347 | 18.2 |
| Quintile 3 | 5,749 | 19.5 |
| Quintile 4 | 5,329 | 18.1 |
| Quintile 5 (highest) | 5,462 | 18.6 |
| Missing | 1,198 | 4.1 |
Lung cancer screening eligibility is based on electronic health record data for people meeting eligibility requirements according to US Preventive Services Task Force 2013 guidelines (ages 55–80 years, current or former smoker, 30+ pack-years smoking history, and < 15 years since quitting smoking).
During the 12 months prior to 9/30/2019, 8,333 (28.3%) of those eligible had a chest CT and were considered up-to-date with testing. About 75.6% had a prior LCS LDCT; 24.4% had a diagnostic or other Chest CT. Percent up-to-date with testing by health system, ranged from 21% to 42%. Compared to individuals ages 55–64 years, 65–74 year-olds were more likely to be up-to-date (PR = 1.19; CI: 1.15–1.24). Living in census tracts with higher SES (PR = 1.22; CI: 1.16–1.30, highest Yost quintile vs. lowest) and having COPD (PR = 2.05; CI: 1.98–2.13) were also positively associated with being up-to-date. Currently smoking (PR = 0.91; CI: 0.88–0.95), having a BMI ≥ 30 kg/m2 (PR = 0.83; CI: 0.77–0.88), and being part of a decentralized LCS program (PR = 0.77; CI: 0.74–0.80) were inversely associated with being up-to-date. Among minoritized racial and ethnic groups, only Hawaiian and Other Pacific Islander individuals were less likely to be up-to-date than White individuals (PR=0.79; CI: 0.68–0.92) (Table 2).
Table 2.
Prevalence ratios of up-to-date with testing among those eligible for lung cancer screening.
| Characteristic | Up-to-date with testinga (%) | Unadjusted Prevalence Ratios (95% CI) | Adjusted Prevalence Ratiosb (95% CI) |
|---|---|---|---|
| Age (years) | |||
| 55 – 64 | 24.0 | [Ref] | [Ref] |
| 65 – 74 | 32.8 | 1.37 (1.31, 1.42) | 1.19 (1.15, 1.24) |
| 75 – 80 | 28.7 | 1.19 (1.13, 1.27) | 0.96 (0.90, 1.01) |
| Sex | |||
| Male | 28.3 | [Ref] | [Ref] |
| Female | 28.4 | 1.00 (0.97, 1.04) | 0.98 (0.95, 1.02) |
| Race or Ethnicity | |||
| Non-Hispanic White | 28.4 | [Ref] | [Ref] |
| Hispanic | 36.1 | 1.27 (1.17, 1.39) | 1.27 (1.16, 1.38) |
| Non-Hispanic Asian | 31.4 | 1.11 (0.99, 1.04) | 1.09 (0.99, 1.21) |
| Non-Hispanic Black | 28.1 | 0.99 (0.94, 1.04) | 1.12 (1.06, 1.19) |
| Non-Hispanic Hawaiian or Other Pacific Islander | 23.6 | 0.83 (0.71, 0.97) | 0.79 (0.68, 0.92) |
| Unknown or Another Race | 24.2 | 0.85 (0.78, 0.93) | 0.89 (0.81, 0.96) |
| Smoking Status | |||
| Formerly Smoked | 30.2 | [Ref] | [Ref] |
| Currently Smoke | 26.3 | 0.87 (0.84, 0.90) | 0.91 (0.88, 0.95) |
| Yost Index Quintile | |||
| Quintile 1 (lowest) | 27.1 | [Ref] | [Ref] |
| Quintile 2 | 26.7 | 0.98 (0.93, 1.05) | 1.03 (0.97, 1.09) |
| Quintile 3 | 27.7 | 1.02 (1.02, 1.08) | 1.04 (0.99, 1.11) |
| Quintile 4 | 29.6 | 1.09 (1.03, 1.16) | 1.13 (1.07, 1.20) |
| Quintile 5 (highest) | 30.7 | 1.13 (1.07, 1.20) | 1.22 (1.16, 1.30) |
| Type of LCS Program | |||
| Centralized | 31.1 | [Ref] | [Ref] |
| Decentralized | 22.6 | 0.73 (0.70, 0.76) | 0.77 (0.74, 0.80) |
| Chronic Obstructive Pulmonary Disease | |||
| No | 21.3 | [Ref] | [Ref] |
| Yes | 45.1 | 2.12 (2.05, 2.20) | 2.05 (1.98, 2.13) |
| Body Mass Index (kg/m2) | |||
| < 25 | 30.9 | [Ref] | [Ref] |
| 25 – 29.99 | 29.0 | 0.94 (0.90, 0.98) | 0.98 (0.91, 1.04) |
| 30 + | 25.7 | 0.83 (0.80, 0.87) | 0.83 (0.77, 0.88) |
Up-to-date with testing is defined as having a chest CT for any indication within the 12 months prior to September 30, 2019.
Mutually adjusted for all factors in Table 2.
Discussion
Results from this study suggest that even among insured populations, the percent up-to-date with testing in the context of LCS remains well below the 65–73% up-to-date estimates for other types of cancer screening.3 Inequity in the percent of the population up-to-date was observed for those in areas with lower SES and for individuals identifying as Hawaiian or Other Pacific Islander. Individuals who were obese, currently smoked, or in healthcare systems with decentralized LCS also had lower LCS participation.
Prior studies estimate that <30% of eligible individuals have received LCS according to the metric, percent of the eligible population screened.8,9 However, this is the first LCS analysis to report on the metric, up-to-date with testing. As Barlow, et al. describes,5 up-to-date with testing estimates “the prevalence of screening coverage in the population” and includes “those receiving testing regardless of indication”. This metric provides a snap-shot of the eligible population not currently in need of screening (because they are up-to-date based on a prior screening or diagnostic test or procedure). HEDIS measures use the up-to-date metric for measuring the quality of other cancer screening programs with USPSTF grade A or B recommendation.3 Given the current grade B recommendation for LCS, a similar quality metric should be considered and evaluated.
Similar to results in the present study, a recent review identified disparities in LCS utilization for those with lower SES.9 In contrast to the present study, this review reported lower LCS utilization for Black compared to White populations. This difference may be due to the centralization of LCS programs within several PROSPR-Lung healthcare systems and because this population was largely insured, thereby reducing some barriers to cancer screening.10 Given disparities in lung cancer mortality and survival by SES and race,11 health systems need to track LCS participation among medically underserved subgroups and ensure that LCS helps to close, and not widen, disparities.
Limitations
This study population included five geographically, racially, and ethnically diverse healthcare systems in the U.S. with strong ascertainment of patient characteristics and chest CTs through comprehensive EHRs. Despite these strengths, results should be interpreted considering the following limitations. PROSPR-Lung is largely an insured population and not necessarily representative of uninsured populations. Additionally, this cohort received care in a participating healthcare system and may be more likely to receive chest CT than individuals not receiving care within a healthcare system. Finally, missing smoking data may have resulted in an under capture of LCS-eligible individuals.
Conclusions
Based on results present here and by others,12 healthcare systems may increase LCS participation through centralized LCS programs. Additional research aimed at identifying quality-based benchmarks for LCS participation is needed to incentivize health systems to find additional ways to increase LCS participation and achieve equity in the utilization of LCS.
ACKNOWLEDGEMENTS
The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Funding Sources:
Research reported in this publication was supported by the National Cancer Institute of the National Institutes of Health under Award Numbers UM1CA221939 (MPI: Ritzwoller/Vachani) and R50CA251966 (PI: Carroll).
Footnotes
Conflict of Interest Disclosures: Dr. Burnett-Hartman reports research funding paid to her institution from Biodesix, outside the submitted work. Dr. Kim reports research funding paid to his institution from Siemens, outside of the submitted work. Dr. Rendle reports grant funding paid to her institution from Pfizer and AstraZeneca, outside of the submitted work, and serves as a paid advisor for Merck, outside of the submitted work. Dr. Vachani reports personal fees as a scientific advisor to the Lung Cancer Initiative at Johnson & Johnson and grants to his institution from MagArray, Inc., Precyte, Inc., and Optellum Ltd. outside of the submitted work. Dr. Vachani is also an advisory board member of the Lungevity Foundation (unpaid). All other authors have no financial disclosures.
CREDIT AUTHOR STATEMENT
ANBH, NMC, and DPR, contributed to the study design, data acquisition, data analysis, results interpretation, and the writing of the manuscript; RTG, SAH, CND, KAR, and AV contributed to study design, data acquisition, results interpretation, and critical revision of the manuscript; JMC and RYK contributed to study design, results interpretation, and critical revision of the manuscript. All authors reviewed and approved of the final draft and agree to be accountable for all aspects of this work.
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