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Abstract
Rationale: The U.S. Preventive Services Task Force recommends annual low-dose computed tomography (LDCT) for lung cancer screening in high-risk individuals. Preventive healthcare is provided predominantly by primary care providers (PCPs). Successful implementation of a screening program requires acceptance and participation by both providers and patients, with available collaboration with pulmonologists.
Objectives: To identify perceptions of and perspectives on lung cancer screening and implementation among PCPs and eligible veteran patients at high risk for lung cancer.
Methods: We conducted a qualitative study using grounded theory in which 28 veterans and 13 PCPs completed a questionnaire and participated in focus groups. Sessions were recorded, transcribed verbatim, and analyzed with NVivo 10 software. Counts and percentages were used to report questionnaire results.
Measurements and Main Results: While 58% percent of providers were aware of lung cancer screening guidelines, many could not recall the exact patient eligibility criteria. Most patients were willing to undergo LDCT screening and identified smoking as a risk factor for lung cancer, but they did not recall their PCP explaining the reason for the testing. All providers assessed smoking behavior, but only 23% referred active smokers for formal cessation services. Patients volunteered information regarding their hurdles with smoking cessation while discussing risk factors for cancer. PCPs cited time constraints as a reason for lack of appropriate counseling and shared decision making. Both parties were willing to explore modalities and decision aid tools to improve shared decision making; however, while patients were interested in individual risk prediction, few PCPs believed statistical approaches to counseling would confuse patients.
Conclusions: While patients and providers are receptive to LDCT screening, efforts are needed to improve guideline knowledge and adherence among providers. System-level interventions are necessary to facilitate time and resources for shared decision making and smoking cessation counseling and treatment. Further research is needed to identify optimal strategies for effective lung cancer screening in the community.
Annual low-dose computed tomography (LDCT) is now recommended for lung cancer screening in high-risk individuals based on age and smoking history (1). Essential components of an effective screening program incorporate both shared decision making and smoking cessation (2), which are also requirements of the Centers for Medicaid and Medicare Services for both accreditation and reimbursement (3).
Primary care providers (PCPs) are the first point of contact with the healthcare system for most adults. They play a critical role in offering preventive healthcare and screening, and help facilitate early diagnosis and appropriate referrals for specialty care services. For successful implementation of a new screening procedure, its indication, risks, and benefits must be understood and accepted by the frontline providers and their patients.
Lung cancer is considered a stigmatizing disease because the majority of cases are attributable to tobacco use, and survivors tend to experience regret and personal responsibility (4). Age, smoking status, and smoking history are the key variables used to identify high-risk individuals who would benefit from screening. Studies conducted prior to the publication of the U.S. Preventive Services Task Force (USPSTF) guidelines showed that current smokers are less interested than never smokers in undergoing lung cancer screening (5) and that veterans are receptive to LDCT screening (6). Since the publication of the National Lung Screening Trial in 2011 (7), several centers have started offering LDCT screening. We conducted this study to elicit perspectives on lung cancer screening within a structured program among PCPs and eligible patients. Preliminary results derived from this study were presented as an abstract at the 2016 American Thoracic Society conference (8, 9).
Lung cancer screening was implemented at the study site starting in 2012 as part of a clinical demonstration project conducted by the Veterans Health Administration (10). A pulmonologist was the site lead for the demonstration project, and a dedicated nurse coordinator was hired. PCPs identified eligible patients for screening through clinical reminders built into the electronic medical record (EMR) and referred them to the program. The nurse coordinator provided patients with information on the risks and benefits of screening, scheduled the scan, relayed results, and tracked screen-detected nodules.
Because limited data was available that described providers’ or veterans’ experiences with screening, constructivist grounded theory was chosen as the appropriate qualitative method (11). This approach provides a way to search for participant meanings recognizing the embedded nature of their experiences within a larger network of relationships that influence their beliefs and assumptions as well as those of their interviewers who were also part of the Veterans Affairs (VA) healthcare system.
This qualitative study consisted of a structured questionnaire to explore participant contexts (see Appendices E1 and E2 in the online supplement) and a moderated focus group discussion to explore perceptions of risk and participation in lung cancer screening. Focus groups were led by personnel trained in group facilitation using open-ended questions based on principles of qualitative interviewing (12) (Appendix E3). Field notes were taken during the focus groups, and they were recorded, transcribed verbatim, and analyzed with NVivo 10 software (QSR International, Doncaster, Australia).
Providers at the Ralph H. Johnson VA Medical Center and outpatient clinics were contacted via e-mail for study enrollment. Thirteen individuals agreed to participate, meeting the number of providers considered adequate to achieve qualitative study thematic saturation (13). To confirm saturation, codes were monitored until no new codes appeared (14, 15).
Veterans meeting USPSTF criteria for lung cancer screening who had been offered LDCT screening by their PCPs were approached via mail and phone. They were offered $35 compensation. Twenty-eight veterans participated in focus group sessions.
All members of the study team reviewed focus group transcripts. Subsequently, two members (N.M.K., L.J.R.) examined the transcripts independently and then jointly coded the transcripts for content analysis (14, 15). A third member (C.P.), an experienced in constructivist grounded theory (11), coded for the broadest perspectives possible. Using content analysis, the coders identified semantic categories based on jointly devised decisions. By contrast, use of constructivist grounded theory began with open coding. Any differences were resolved by consensus. This study was approved by the institutional review board at the Medical University of South Carolina (Pro00030926).
PCP and patient focus groups were analyzed separately, and the generated themes were subsequently aligned to develop a cohesive understanding of experiences with lung cancer screening among participants on both sides of the healthcare system. Table 1 outlines the patient demographics. PCP demographic information was not collected. The themes were (1) awareness, (2) providers’ approach to offering and communicating screening to eligible patients and veterans’ rationale underlying their screening decision, (3) smoking cessation, and (4) suggestions to improve shared decision making.
| Variable | Data |
|---|---|
| Median age, yr (interquartile range) | 65 (55–76) |
| Sex | |
| Male | 28 (100%) |
| Female | 0 (0%) |
| Race | |
| White | 11 (39.3%) |
| African American | 16 (57.1%) |
| Prefer not to answer | 1 (3.6%) |
| Marital status | |
| Married | 18 (64.3%) |
| Other (single/divorced/widowed/separated) | 10 (35.7%) |
| Work status | |
| Employed full time | 6 (21.4%) |
| Retired/not working | 22 (78.6%) |
| Education | |
| Less than high school | 5 (18%) |
| High school or greater | 23 (82%) |
The questionnaire indicated that all PCP participants had screened patients for lung cancer with chest X-rays or LDCT in the past 12 months. More than half (58%) indicated awareness of USPSTF guidelines. During provider focus group discussions, there was agreement about lung cancer screening; however, there was variation in commitment and enthusiasm for it. Responses ranged from screening because “I do whatever my VA tells me to do” to being in favor of screening: “I think it’s evidence based and patients are receptive to it.” Most providers, however, were unable to immediately recall screening eligibility criteria and instead relied on alerts embedded in the EMR. Some expressed concern about the presence of multiple lung cancer screening guidelines and mentioned that it was challenging to keep up with the details at all times.
The majority of veteran participants identified smoking as a risk factor and were also concerned about exposure to other risks: “I’m a smoker for 50 years myself. I work in construction and exposed to asbestos, so I feel like I’m at risk.” The degree to which they believed smoking contributed to their risk, however, varied: “I smoke, but I barely inhale, so it’s sort of like, it ain’t gonna bother me. That’s my way of thinking.” Other veterans identified previous inhalational exposures as increasing their risk of lung cancer, but identified smoking as the primary risk factor: “Ah, I don’t know, because of my past, I had pesticides, chemicals, plus I’m a heavy smoker, a pack of cigarettes [a day]. That’s the main thing.”
While discussing their approach to assessing patient eligibility and offering screening, providers stated that they relied on the clinical reminder generated by the EMR to identify high-risk individuals. Those providers who discussed the reasons for lung cancer screening focused on the evidence for screening: “I tell them it’s based on a huge study that was done. We have a lot of evidence to support [screening].”
A minority explained to patients that screening was done with a low-radiation computed tomographic (CT) scan. While some reported initiating a discussion about risks and benefits of LDCT screening, others preferred that the screening coordinator review those details, incidental findings, and the possibility of continued surveillance imaging. They cited time constraints of a primary care follow-up appointment as the reason for this: “I mean, I just don’t have the time to go in detail about lung cancer to that depth … because, to be quite honest, some of that workload just [needs] to be offloaded.”
PCPs observed that the majority of patients were receptive and willing to undergo a CT scan; a minority declined the test because of fear of being diagnosed with cancer or some other respiratory illness. Another reason for refusal recalled by providers was the copay ($50) for the LDCT scan.
The National Center for Health Promotion and Disease Prevention had designed a decision aid brochure outlining the risks and benefits of lung cancer screening, which was made available to screening sites. The majority of PCPs were unaware of the brochure or that it was mailed to patients prior to LDCT screening.
Several PCPs reported that patients with a recent cancer death in the family and those with heavy smoking histories would inquire about cancer screening and request imaging. “Well, the ones who smoke a lot, they’re always wanting chest X-rays, but I’m, like, why? Quit smoking.” Others also noted that in this veteran population some patients suspected they were being offered screening because of exposures during military service. “Are you doing that because of something, like Agent Orange? I get that a lot, actually.”
Many providers stated that no patients had asked about their individual risk for developing lung cancer. Patients also did not ask questions related to potential LDCT scan findings, follow-up testing, or steps to be taken if the scan showed cancer. Alternatively, they felt that patients viewed undergoing CT as noninvasive and were met with little resistance, resulting in truncated discussions of risks and benefits: “I’ve actually had a difficult time [discussing risks and benefits] because once—so many screening tests are unpleasant that once you let them know that it’s just a CAT scan, usually—they’ll actually shut down and say, ‘Okay, let’s do it.’ And I can’t communicate to them the fact that no, no, no. You may not actually not want to do this, you know. It may not be a good thing for you.”
Patients reported having a trusting relationship with their PCPs and were receptive to screening discussions with their providers despite the fact that only 61% believed that they were at risk for lung cancer. Most patients, however, did not recall having a detailed discussion about LDCT screening with their PCP. “They asked me to come and do a screen, a CT deal. So, I drove up here, you know, I live 80 miles from here. I drove up here, and … why am I doing this? Oh, Dr. — ordered it. Really? He never mentioned to me that he [was] ordering this.” They did, however, find the conversation with the coordinator helpful: “The lady on the phone gave me more information than the doctor did.”
In addition to risk of disease, test accuracy and screening convenience were factors listed as being of highest priority to patients and reasons for declining screening. While veterans received the shared decision aid, many admittedly did not read it. Those who did used the information to make their decision: “But after reading the brochure, I decided I didn’t want to do this, because I know how I feel now, and in that article it told you that there could be some false readings.”
Discussions related to guidelines, risks, and benefits of screening as well as patient responsiveness evoked comments related to smoking. Providers reported asking their patients about cigarette smoking, but only 23% made referrals to the local cessation clinic and quit lines. The majority of the providers experienced challenges in modifying the smoking behavior of heavy, current smokers: “Well, I think the big problem is they think ‘It’s not gonna happen to me.’” They reported that patients were optimistic about their own health, felt that they would not get cancer, or had anecdotes about smokers they knew who lived long and healthy lives.
Providers noted that some patients were resistant to discussing smoking cessation but were agreeable to undergoing an imaging study. “So, usually, they’re like, sure, let’s do it. But they don’t want to quit smoking. But they are happy to do [LDCT].” PCPs admitted to not devoting enough time to smoking cessation counseling, given competing health conditions that demanded their immediate attention: “I mean, we, you know, there’s so many problems to deal with, I mean, smoking is just like a 30-second thing. I mean, you know, it should be more, but we just don’t have time to address those in great detail with patients, unfortunately.”
Many patients volunteered their experiences with smoking and the challenges they faced during quit attempts. They recalled consistent messages from all healthcare team members about smoking cessation, but some reported being diagnosed with a noncancer smoking-related illness that prompted them to quit: “Well, this is what I can do for you…. I can do this, and if you continue to smoke, I might have to cut your leg off one day…. And I say, okay, I went outside, threw all my cigarettes away, and I haven’t touched one since.” They also reflected on how tobacco was an addiction difficult to overcome: “If a person wants to smoke, I don’t care if you showed him a hundred movies or told them, you know, he’s gonna die tomorrow, he gonna light up because that’s how I did it.” As observed by the PCPs, the majority of patient participants (71%) perceived their own health to be good, very good, or excellent compared with their age cohort.
Many providers reported not having sufficient time or information to have in-depth discussions related to screening. They found the current system of EMR-embedded reminders with subsequent referral to the screening coordinator, who then followed up on results and managed downstream testing, to be effective and convenient: “I mean, I think that the way you do it now is very good because all I need to do is just click a couple of boxes, and I’m done with it.” They felt that posters in the waiting area, streaming videos, and availability of decision aids in the clinic may help facilitate conversations about lung cancer screening.
Providers were asked about their thoughts on using personalized lung cancer risk prediction calculators. A few felt that this aid would hinder decision making because abstract statistics are not easy to apply to an individual patient and may obscure the importance of screening. Some providers had a poor understanding of risk prediction themselves: “And what I tell people is, you know, the truth is absolute, you’re gonna get something or you’re not gonna get something. You know, so your risk is always 50%.”
Most PCPs also felt that guideline dissemination and dedicated personnel to review screening findings and offer smoking cessation would be needed to operationalize lung cancer screening: “I think we have so many guidelines that it’s hard to be able to focus on any one at any particular time. Sometimes we do have to educate ourselves….” “I’ve had people who refused medications or [smoking] treatment, and then they have accepted them when [screening coordinators] called them.”
The majority of patients reported having a trusting relationship with their PCP who was aware of their overall health status, but they valued the in-depth interaction with the screening coordinator. “[The screening coordinator] explained it in great details on the phone about the false stuff, the person that talked to me, did that really in detail.” They were receptive to more information about the pros and cons of screening and felt that educational content by way of brochures, posters, or videos would be most helpful in the waiting area prior to a clinic visit: “[L]ike a video. Or a DVD. People might say, ‘Hey, look at it.’” They stated that when the brochure was mailed to them, they paid less attention to it, but they found it informative while reviewing it during the focus group. They were open to understanding their individual risk through risk calculators: “I think just get out the statistics, you know. Show them however many people … smoke over x period of time. This many get lung cancer or other issues like emphysema, something like that.” Overall, study participants expressed enthusiasm for lung cancer screening: “You need to … make the program serious. Let’s just don’t do this to appease somebody. If you gonna do this … long-standing …, put everything you got into it.… So, you gotta get people some information and let them make the decision.”
In this study, we sought to understand the experiences with and perceptions of lung cancer screening among practitioners and patients at a site where a structured lung cancer screening program was implemented. Our study has several important findings. First, both PCPs and patients had limited knowledge of screening test characteristics. Second, the integration of lung cancer screening and smoking cessation was considered important to all, but systematic referral to cessation services was less undertaken. Third, providers felt that time constraints prevented them from providing in-depth discussions about LDCT screening and preferred that this step be done by a dedicated screening coordinator; this sentiment was echoed by patients. Finally, some discordance exists between providers and patients as it relates to gathering and understanding information prior to participating in lung cancer screening. These findings suggest that improvements in provider and patient knowledge about LDCT screening are needed to ensure successful population-based implementation.
Despite having been in-serviced prior to the initiation of screening at the site (2012), most PCPs were unsure of exact eligibility criteria, and 58% were aware of USPSTF guidelines (1). Some continued to believe that a chest X-ray is effective for screening, and one-third had ordered one in the past year. These findings are in line with recent studies demonstrating that some family physicians as well as academic center PCPs are unaware of lung cancer screening guidelines and that others continue to screen for lung cancer using chest X-rays (16–18). Our study adds to growing evidence of the need to improve guideline dissemination to and adoption by PCPs.
From a patient perspective, variables of highest importance when deciding to undergo screening included test accuracy, convenience, and cost. These findings parallel those of prior studies (5, 6, 19). The majority of patients agreed to undergo LDCT screening; however, many were unaware of why they were being screened and could not communicate the risks or benefits of the test.
Surveys have shown that most Americans undergoing cancer screening do not engage in a balanced discussion meeting criteria for shared decision making with their providers (20). However, shared decision making is promoted as an essential aspect of healthcare delivery (21). Our study and others have identified lack of time and competing priorities as potential barriers to effective lung cancer screening (18) and shared decision making. PCPs preferred that such discussions be deferred to the screening coordinator, and patients, while trusting of their PCPs overall, agreed that discussion with the coordinator resulted in a more in-depth understanding of the screening process.
Tobacco cessation within lung cancer screening was another theme that emerged in this study. While it is reassuring that all providers took the time to elicit smoking history, there is opportunity to improve cessation counseling and referral. An analysis of the National Lung Screening Trial population showed that 77% of participants continued to smoke after three rounds of screening (22). A recent qualitative study showed that offering lung cancer screening may exacerbate misperceptions about smoking and negatively influence cessation (23). Another study showed that 7 years of smoking cessation provided mortality benefits comparable to those of annual LDCT screening, and, when combined with screening, the benefit was even greater (24).
Both smoking cessation and shared decision making are key components of lung cancer screening and are required by the Centers for Medicaid and Medicare Services for accreditation and reimbursement (3). Our study shows that these two aspects of the screening process are challenging for PCPs to achieve and that patients’ needs are not met completely. Thus, screening services may be more effective if offered in a freestanding program where multidisciplinary teams and appropriate infrastructure can be brought to bear (2, 25).
Last, our study demonstrates an important area of discordance between what PCPs believed to be true for their veteran patients and what veterans preferred. Although patients were receptive to the idea of using risk prediction tools to help them understand individual risk for developing lung cancer, some providers were not enthusiastic, citing the reason that use of these tools had the potential to confuse patients. A systematic review evaluating tailored risk communication demonstrated that personalized risk assessment increases screening knowledge and uptake and provides a more accurate personal risk perception among patients (26). In addition, comments made by providers demonstrated that some had poor understanding of risk prediction and relayed inaccurate messages to their patients. This observation is supported by prior survey studies which showed that physicians’ interpretation of trial statistics is often inaccurate (27) and that providers’ risk communication is unbalanced (20).
Our study has limitations. First, we used a convenience sample with only a few screening decliners. While the sample size was small, it met criteria for thematic saturation in a qualitative study. Second, recall bias may have affected participants’ responses. Third, all participants were part of the VA healthcare system, and all patient participants were male, so the findings may not be generalizable to other providers and patients.
In conclusion, efforts are needed to disseminate lung cancer screening guidelines effectively among PCPs. Given the time constraints of a busy clinical practice, system-level interventions are required to emphasize shared decision making and ensure that smoking cessation services are embedded in lung cancer screening programs. While better guideline dissemination and efforts to improve knowledge among providers are needed, one possible solution is the use of an integrated lung cancer screening program with personnel trained in its nuances, with added expertise and time to conduct smoking cessation and risk-benefit counseling. Given the various domains of an effective lung cancer screening program, further research is required to discern the optimal strategies and preferred setting for its effective implementation in the community.
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Supported by the Veterans Affairs (VA) Health Equity and Rural Outreach Innovation Center (HEROIC) at the Ralph H. Johnson VA Medical Center, Charleston, SC.
Author Contributions: Conception and design of the study: N.T.T., C.P., C.H.H., and G.A.S.; study implementation: N.T.T., N.M.K., C.P., and C.H.H.; analyses: N.M.K., C.P., L.J.R., C.H.H., and N.T.T.; and drafting and editing of the manuscript: N.M.K., C.P., L.J.R., C.H.H., G.A.S., and N.T.T.
This article has an online supplement, which is accessible from this issue’s table of contents at www.atsjournals.org
Author disclosures are available with the text of this article at www.atsjournals.org.
