More patients die of lung cancer than breast, colorectal, and prostate cancers combined (1). After the National Lung Screening Trial finding of a 20% relative reduction in mortality of lung cancer with lung cancer screening (LCS) by low-dose computed tomography (LDCT) (2), the U.S. Preventive Services Task Force published recommendations for LCS in high-risk patients (current and former heavy smokers aged 55–80 yr) annually with LDCT (3)

Bearden, S.C.

Benefield, T.S.

Brenner, A.T.

Goldstein, A.O.

Henderson, L.M.

Reuland, D.S.

Rivera, M.P.

Throneburg, A.

Carolina Digital Repository

LETTERSChanges in Physician Knowledge, Attitudes, Beliefs,and Practices regarding Lung Cancer ScreeningTo the Editor:More patients die of lung cancer than breast, colorectal, andprostate cancers combined (1). After the National LungScreening Trial finding of a 20% relative reduction in mortality oflung cancer with lung cancer screening (LCS) by low-dosecomputed tomography (LDCT) (2), the U.S. Preventive ServicesTask Force published recommendations for LCS in high-riskpatients (current and former heavy smokers aged 55–80 yr)annually with LDCT (3).Eligibility for LCS is based on age, pack-years of smokinghistory, and years since quitting, with reimbursementdependent on physician and patient engagement in shareddecision making (SDM). Rates of LCS from 2013 to 2016 werelow, ranging from 2% to 7% (4, 5). To understand reasons for lowLCS rates, several studies have examined physician attitudesand beliefs regarding screening (6–14). However, these studieswere cross-sectional and conducted at a single time point.Isolated snapshots may not accurately reflect provider changes inLCS attitudes and practices. To assess changes in physicians’knowledge, attitudes, and practice patterns regarding LCSover time, we redeployed our 2015 LCS physician opinionsurvey (6, 15) in 2018 to compare two cross-sectional cohortsof physicians.MethodsUsing the Tailored Design Method, we conducted a Qualtricssurvey of physicians in family medicine, internal medicine, andpulmonary medicine at a large academic medical center in thespring of 2015 and in the spring of 2018 (16). We included 23survey items focused on LCS opinions, knowledge, practices, andperceived barriers. Physicians’ LCS opinions were evaluated using a5-point Likert scale that ranged from strongly agree to stronglydisagree. Physicians were asked to rank their opinions on sixstatements (Figure 1). Physician practice pattern survey questionsasked about behaviors in the prior 12 months with response optionsof yes, no, or don’t recall (Figure 2) and a single question aboutreferrals for smoking cessation programs. To ascertain physicians’perceived barriers to LCS, we provided a list of potential barriers(Figure 3) and asked physicians to select all perceived barriers.We identified physicians through online academic directoriesand made seven points of contact per the Tailored DesignMethodology. Consent was determined by return of the survey.Participating physicians were incentivized with the opportunity toenter into a random drawing for an iPad. This study was approvedby the University of North Carolina at Chapel Hill InstitutionalReview Board (approval no. 13-2672).Between the two surveys, we implemented a qualityimprovement project to address key processes required for high-quality LCS implementation (17, 18) and disseminated LCSresources to physicians. We conducted outreach to primary careproviders in outpatient clinics, providing written educationalmaterials pertaining to LCS and tobacco treatment as well asdemonstrating web-based SDM tools.We compared responses from physicians in 2015 with those in2018 using t tests for continuous outcomes and chi-square orFisher’s exact tests for categorical outcomes. We accounted formultiple comparisons by adjusting all P values using the falsediscovery rate method (19).ResultsSurvey response rates were 40.5% (89 of 220) in 2015 and 30.0% (73of 243) in 2018. There were no differences in the distribution ofage, sex, race, years in clinical practice, or proportion of time spentin outpatient care or in the average number of outpatients seen perweek for respondents in 2015 versus 2018. The proportions ofrespondents in family medicine were 41.6% in 2015 and 43.8% in2018; in internal medicine, they were 39.5% in 2015 and 39.3% in2018; and in pulmonary medicine, they were 19.1% in 2015 and16.4% in 2018. Over time, there was an increase in the proportion ofphysicians who reported LCS as beneficial (47.7% vs. 77.2%;adjusted P, 0.01) (Figure 1). In both years, approximately half ofrespondents were undecided on the cost effectiveness of LCS(56.3% and 48.6%, respectively; adjusted P= 0.09), and most of therespondents believed they had enough knowledge to explain thepros and cons of LCS (64.7% in 2015 and 75.7% in 2018; adjustedP= 0.49). Approximately two-thirds of physicians cited timerestrictions during the patient’s clinic visit and other problemshaving higher priority than LCS (62.3% in 2015 and 70.0% in 2018;adjusted P= 0.49).Over the 3 years between 2015 and 2018, the proportion ofphysicians who reported initiating LCS discussions increased from45.9% to 87.3% (adjusted P= 0.03), and the proportion whoreported ordering an LCS examination more than doubled (from32.2% to 74.6%; adjusted P= 0.02) (Figure 2). The proportion ofphysicians who referred a patient to another provider for LCSevaluation also increased (12.9% in 2015 vs. 29.9% in 2018; adjustedP= 0.03).The proportion of physicians who reported any barrier toLCS was similar: 89.9% in 2015 and 86.3% in 2018 (Figure 3).Although many physician-reported barriers to LCS remained constantover time, fewer physicians reported lack of evidence (adjustedP=0.05)or patient cost (adjusted P=0.03) as a barrier in 2018 than in 2015.DiscussionWe found significant increases between 2015 and 2018 in theproportion of physicians who reported initiating a discussion aboutLCS, ordering LDCT for LCS, discussing LDCT results, andreferring patients for further evaluation. In contrast, physicians(Received in original form December 7, 2018; accepted in final form May 10,2019 )Supported by the National Cancer Institute at the National Institutes of Health(grant 1R01CA212014-01A1).Author Contributions: L.M.H.: conceptualization, methodology, software,resources, supervision, project administration, funding acquisition, writing ofthe original draft, and review and editing. T.S.B.: data curation, methodology,formal analysis, software, and review and editing. S.C.B.: data curation, projectadministration, and review and editing. D.S.R.: resources and review andediting. A.O.G.: resources and review and editing. A.T.: resources and reviewand editing. M.P.R.: conceptualization, funding acquisition, writing of theoriginal draft, and review and editing.Letters 1065 reported a similar proportion of patients asking about LCS,suggesting that physicians have gained knowledge and experiencein LCS, whereas patients’ knowledge regarding LCS has notchanged. This is an area for future investigation.According to physician respondents, barriers to LCSremain a concern, with few barriers decreasing over time.Other studies reported similar barriers at a single time point (9, 10,12, 13, 20–22). Because of the complexities of LCS, physiciansfind it increasingly challenging to allocate their alreadylimited time and resources to incorporate the necessaryand required components of LCS (patient eligibility assessment,benefit and risk discussion coupled with SDM, anddiscussion/referral/treatment for tobacco addiction) intodaily practice. To accomplish widespread acceptance ofLCS, physician education and system-level changes are required(23, 24).100%80%60%40%20%0%A2015 (n=89)Strongly Agree Agree Undecided Disagree Strongly Disagree2018 (n=73)Inconsistent recommendations about lung cancer screeningmake it difficult to decide whether or not to screenB100%80%60%40%20%0%2015 (n=89)Strongly Agree Agree Undecided Disagree Strongly Disagree2018 (n=73)Screening for lung cancer is cost-effectiveC100%80%60%40%20%0%2015 (n=89)Strongly Agree Agree Undecided Disagree Strongly Disagree2018 (n=73)I rely on the recommendations of localspecialists regarding lung cancer screening in my practiceD100%80%60%40%20%0%2015 (n=89)Strongly Agree Agree Undecided Disagree Strongly Disagree2018 (n=73)I have enough knowledge to explain the prosand cons of lung cancer screening to my patientsE100%80%60%40%20%0%2015 (n=89)Strongly Agree Agree Undecided Disagree Strongly Disagree2018 (n=73)Time restrictions during a patient’s clinic visitmean other presenting problems have higher priority thanscreening for lung cancerF100%80%60%40%20%0%2015 (n=89)Strongly Agree Agree Undecided Disagree Strongly Disagree2018 (n=73)I am convinced that lung cancer screening is beneficial for patientsFigure 1. (A–F ) Comparison of physicians’ lung cancer screening opinion statements from 2015 and 2018.1066 AnnalsATS Volume 16 Number 8| August 2019LETTERS Our survey was implemented using the Tailored DesignMethod, a standard survey methodology that is rigorous interms of survey design and deployment. Our response rates aresimilar to those for other nonspecialty physician surveys focusedon LCS (range from 7% to 53% [7, 9, 11, 13, 20, 22, 25]), althoughour sample sizes are modest. It is possible that attitudes andpractice patterns at our single site may not represent nationalpatterns.We found that physicians view LCS as more beneficial andwere more likely to order LDCT for LCS in 2018 than in 2015;however, physicians continued to have concerns regarding timerestrictions and other barriers to LCS. This research has implicationsfor continued adoption and dissemination of LCS into practice. As LCScontinues to gain momentum in the United States and withpreliminary results of the Nelson Lung Cancer Screening Trial favoringLCS (26), identifying and addressing barriers to LCS are needed.Author disclosures are available with the text of this letter atwww.atsjournals.org.Louise M. Henderson, Ph.D.*Thad S. Benefield, M.S.S. Caitlin Bearden, M.S.W.Daniel S. Reuland, M.D., M.P.H.Alison T. Brenner, Ph.D.Adam O. Goldstein, M.D.Allison Throneburg, B.S.M. Patricia Rivera, M.D.University of North CarolinaChapel Hill, North CarolinaIn the last 12 months, did any of your patientsask if they should be screened for lung cancer with LDCT?100%A80%60%40%20%0%2015 (n=89)Yes No Don't Recall2018 (n=73)BYes No Don't Recall100%80%60%40%20%0%2015 (n=89) 2018 (n=73)CYes No Don't Recall100%80%60%40%20%0%2015 (n=89) 2018 (n=73)In the last 12 months, did you discuss results ofLDCT for lung cancer screening?DYes No Don't Recall100%80%60%40%20%0%2015 (n=89) 2018 (n=73)In the last 12 months, did you refer patient toanother provider for evaluation of lung cancer screening?EYes No Don't Recall100%80%60%40%20%0%2015 (n=89) 2018 (n=73)In the last 12 months, did you initiate lung cancer screeningdiscussion re benefits/harms?In the last 12 months, did you order LDCT forlung cancer screening?Figure 2. (A–E ) Lung cancer screening practice statements from 2015 and 2018. LDCT= low-dose computed tomography.Letters 1067LETTERS ORCID ID: 0000-0001-8356-9267 (L.M.H.).*Corresponding author (e-mail: louise_henderson@med.unc.edu).References1 Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018.CACancer J Clin2018;68:7–30.2 Aberle DR, Adams AM, Berg CD, BlackWC, Clapp JD, Fagerstrom RM,et al.; National Lung Screening Trial Research Team. Reduced lung-cancer mortality with low-dose computed tomographic screening.N Engl J Med 2011;365:395–409.3 Moyer VA; U.S. Preventive Services Task Force. Screening for lungcancer: U.S. Preventive Services Task Force recommendationstatement. Ann Intern Med 2014;160:330–338.4 Huo J, Shen C, Volk RJ, Shih YT. Use of CT and chest radiography forlung cancer screening before and after publication of screeningguidelines: intended and unintended uptake. JAMA Intern Med 2017;177:439–441.5 Li J, Chung S, Wei EK, Luft HS. New recommendation and coverage oflow-dose computed tomography for lung cancer screening: uptakehas increased but is still low. BMC Health Serv Res 2018;18:525.6 Henderson LM, Jones LM, Marsh MW, Brenner AT, Goldstein AO,Benefield TS, et al. Opinions, practice patterns, and perceivedbarriers to lung cancer screening among attending and residentprimary care physicians. Risk Manag Healthc Policy 2018;10:189–195.7 Ersek JL, Eberth JM, McDonnell KK, Strayer SM, Sercy E, Cartmell KB,et al. Knowledge of, attitudes toward, and use of low-dose computedtomography for lung cancer screening among family physicians.Cancer 2016;122:2324–2331.8 Volk RJ, Foxhall LE. Readiness of primary care clinicians toimplement lung cancer screening programs. PrevMed Rep 2015;2:717–719.9 Raz DJ, Wu GX, Consunji M, Nelson R, Sun C, Erhunmwunsee L,et al. Perceptions and utilization of lung cancer screeningamong primary care physicians. J Thorac Oncol 2016;11:1856–1862.10 Hoffman RM, Sussman AL, Getrich CM, Rhyne RL, Crowell RE, TaylorKL, et al. Attitudes and beliefs of primary care providers in NewMexico about lung cancer screening using low-dose computedtomography. Prev Chronic Dis 2015;12:E108.11 Duong DK, Shariff-Marco S, Cheng I, Naemi H, Moy LM, Haile R, et al.Patient and primary care provider attitudes and adherence towards86.357.361.650.74839.738.417.85.589.978.765.258.457.352.838.2369Any BarrierCost to PatientToo Many False PositivesPotential for EmotionalHarmPotential for ComplicationsCost to Health CareSystemLow Patient AcceptanceLack of EvidenceFalse Negatives/Missed CancersPercentage Reporting Barrier2015 (n=89) 2018 (n=73)Figure 3. Physician-reported barriers to lung cancer screening in 2015 versus 2018.1068 AnnalsATS Volume 16 Number 8| August 2019LETTERS lung cancer screening at an academic medical center. Prev Med Rep2017;6:17–22.12 Henderson S, DeGroff A, Richards TB, Kish-Doto J, Soloe C,Heminger C, et al. A qualitative analysis of lung cancer screeningpractices by primary care physicians. J Community Health 2011;36:949–956.13 Lewis JA, Petty WJ, Tooze JA, Miller DP, Chiles C, Miller AA, et al. Low-dose CT lung cancer screening practices and attitudes amongprimary care providers at an academic medical center. CancerEpidemiol Biomarkers Prev 2015;24:664–670.14 Rajupet S, Doshi D, Wisnivesky JP, Lin JJ. Attitudes about lung cancerscreening: primary care providers versus specialists. Clin LungCancer 2017;18:e417–e423.15 Henderson LM, Marsh MW, Benefield TS, Jones LM, Reuland DS,Brenner AT, et al. Opinions and practices of lung cancer screening byphysician specialty. N C Med J 2019;80:19–26.16 Dillman DA, Smyth JD, Christian LM.Internet, mail and mixed-modesurveys: the tailored design method. 3rd ed. Hoboken, NJ: Wiley;2009.17 Cubillos L, Brenner AT, Birchard K, Henderson LM, Molina PL,Pignone M, et al. Multidisciplinary quality improvement initiative tostandardize reporting of lung cancer screening. Trans Lung CancerRes 2018;7(Suppl 3):S297–S301.18 Brenner AT, Cubillos L, Birchard K, Doyle-Burr C, Eick J, HendersonL, et al. Improving the implementation of lung cancer screeningguidelines at an academic primary care practice. J Healthc Qual 2018;40:27–35.19 Benjamini Y, Hochberg Y. Controlling the false discovery rate: apractical and powerful approach to multiple testing. J R Stat SocSeries B Stat Methodol 1995;57:289–300.20 Eberth JM, McDonnell KK, Sercy E, Khan S, Strayer SM, DievendorfAC, et al. A national survey of primary care physicians: perceptionsand practices of low-dose CT lung cancer screening. Prev Med Rep2018;11:93–99.21 Iaccarino JM, Clark J, Bolton R, Kinsinger L, Kelley M, Slatore CG, et al.A national survey of pulmonologists’ views on low-dose computedtomography screening for lung cancer. Ann Am Thorac Soc 2015;12:1667–1675.22 Simmons J, Gould MK,Woloshin S, Schwartz LM,Wiener RS. Attitudesabout low-dose computed tomography screening for lung cancer: asurvey of American Thoracic Society clinicians.Am JRespir Crit CareMed 2015;191:483–486.23 Fintelmann FJ, Bernheim A, Digumarthy SR, Lennes IT, Kalra MK,Gilman MD, et al. The 10 pillars of lung cancer screening: rationaleand logistics of a lung cancer screening program. Radiographics2015;35:1893–1908.24 U.S. Preventive Services Task Force. Lung cancer: screening: finalrecommendation statement. Rockville, MD: USPSTF ProgramOffice, 2013 [accessed 2018 Nov 21]. Available from: https://www.uspreventiveservicestaskforce.org/Page/Document/RecommendationStatementFinal/lung-cancer-screening.25 Raz DJ, Wu GX, Consunji M, Nelson RA, Kim H, Sun CL, et al.The effect of primary care physician knowledge of lungcancer screening guidelines on perceptions and utilizationof low-dose computed tomography. Clin Lung Cancer 2018;19:51–57.26 De Koning H, Van Der Aalst C, Ten Haaf K, Oudkerk M. Effectsof volume CT lung cancer screening: mortality results of theNELSON randomised-controlled population based trial [abstract].J Thoracic Oncol 2018;13(10 Suppl):S185.Copyright © 2019 by the American Thoracic SocietyInfluence of County Sampling on Past Estimates ofLatent Tuberculosis Infection PrevalenceTo the Editor:The National Health and Nutrition Examination Survey(NHANES) has tested for Mycobacterium tuberculosis infectionthree times: in 1971–1972, 1999–2000, and 2011–2012. Based ontuberculin skin test results, the estimated national prevalence oflatent tuberculosis infection (LTBI) among adults was 11–18% in1971–1972 but has remained less than or equal to 6% insubsequent NHANES cycles (1–4). A single 2-year NHANEScycle is designed to produce accurate and stable estimates forconditions with at least 10% prevalence in the noninstitutionalizedcivilian U.S. population (5–7), suggesting that NHANES mightno longer be as nationally representative for LTBI as it is formore common health conditions. Approximately 30 countieswere selected for each 2-year cycle (5). We wished to examinewhether persons in selected counties might have beensystematically more or less likely to have a positivetuberculin skin test result than their counterparts in theapproximately 3,100 counties that were not selected forNHANES participation.MethodsWe created a non-NHANES dataset with demographic profilesand tuberculosis data for all 3,143 U.S. county equivalents(Table 1). The U.S. Census Bureau and Department ofAgriculture websites provided each county’s populationsize and racial/ethnic composition, rural versus urbanclassification, and poverty prevalence for 1970 through 2013.The National Tuberculosis Surveillance System provided annualtuberculosis disease incidence, with the U.S. Census Bureau’sCurrent Population Survey providing county populationdenominators.We also used genotyping results to derive an estimate ofLTBI prevalence for each county. Briefly, this simple back-calculation method assumed that tuberculosis cases notattributed to recent transmission (i.e., based on genotypingresults) instead arose from preexisting LTBI. Then a 0.1%annual risk of reactivation was used to derive an estimatednumber of county residents with untreated longstanding LTBI(8). This county-level LTBI estimation method has not beenThis is publicly funded research by employees of the Centers of DiseaseControl and Prevention (M.B.H., K.M.R., A.N.H., T.R.N., C.A.W.). Alsosupported by an existing U.S. Agency for International DevelopmentIntergovernmental Personnel Act agreement with Emory University(K.G.C.) and a K24 grant (1K24AI114444) funded by National Institute ofAllergy and Infectious Diseases, National Institutes of Health, U.S.Department of Health and Human Services (N.R.G.). The findings andconclusions in this research letter are those of the authors and do notnecessarily represent the official position or views of the Research DataCenter, the National Center for Health Statistics, or the Centers forDisease Control and Prevention.Author Contributions: M.B.H. conceptualized the analysis, and all of theauthors contributed to its design. M.B.H. and K.M.R. created the non–National Health and Nutrition Examination Survey county-level dataset.M.B.H. executed the analysis and prepared the first draft of the article withinthe National Center for Health Statistics Research Data Center. All of theauthors provided critical revisions and approved the final version of themanuscript.Letters 1069LETTERS 

Changes in Physician Knowledge, Attitudes, Beliefs, and Practices regarding Lung Cancer Screening

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Changes in Physician Knowledge, Attitudes, Beliefs, and Practices regarding Lung Cancer Screening

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