Abstract
Objective
Screening for lung cancer with low dose computed tomography aims to reduce lung cancer mortality, but there is a lack of knowledge about how target populations consider its potential benefits and harms.
Methods
We conducted a systematic review of primary empirical studies published in any jurisdiction since 2002 using an integrative meta-synthesis technique. We searched six health and social science databases. Two reviewers independently screened titles, abstracts, and potentially eligible full-text studies. Quantitative assessments and open-ended perspectives on benefits and harms were extracted and convergently integrated at analysis using a narrative approach. Study quality was assessed.
Results
The review included 26 quantitative, 18 qualitative, and 5 mixed methods studies. Study quality was acceptable. Lung cancer screening was widely perceived to be personally beneficial for early detection and reassurance. Radiation exposure and screening accuracy were recognised as harms, but these were frequently considered to be justified by early detection of lung cancer. Stigma, anxiety, and fear related to screening procedures and results were pervasive among current smokers. People with low incomes reported not participating in screening because of potential out-of-pocket costs and geographic access.
Conclusions
Populations targeted for lung cancer screening tended to consider screening as personally beneficial and rationalised physical, but not psychological, harms. Screening programmes should be clear about benefits, use non-stigmatising design, and consider equity as a guiding principle.
Introduction
Lung cancer is the second-most incident cancer and leading cause of cancer mortality globally.1,2 In 2020, an estimated 2.2 million people were newly diagnosed with lung cancer, accounting for 11% of incident cancers that year. 2 Incidence and mortality are increasing among women3,4 and people aged 50 years and older. 4 In high-income countries, rates are higher among current smokers,5,6 those with low socioeconomic status, 7 certain indigenous populations,8,9 and racially minoritised people. 7 Most lung cancers are diagnosed at advanced stages 10 when treatment options are limited and treatment effectiveness is poor, resulting in low survival rates. 11
Risk factors for lung cancer include exposure to lung carcinogens and genetic factors, among others. 1 In 2017, some 63% lung cancer deaths globally were attributed to tobacco smoking, 12 although a growing number of cases occur in people who have never smoked.1,2 Primary prevention has prioritised reducing exposure to lung carcinogens such as tobacco 13 and air pollution, 14 but the disease continues to be diagnosed at high rates worldwide with poor prognosis. It is in this context that countries are increasingly introducing population-based lung cancer screening programmes, using, mostly, low dose computed tomography (LDCT) to detect lung cancer in early stages. 15 Evidence about the effectiveness of screening on lung cancer mortality is still emerging. Trial evidence points to significant reductions in relative mortality,16–18 although the effects on absolute mortality remain small (0.4% in a meta-analysis of eight trials). 19
While lung cancer screening may be cost-effective for some populations, 20 it includes harms. The effectiveness of correctly identifying true cases of lung cancer (sensitivity) ranges from 59 to 100%, and the true absence of lung cancer (specificity) from 26 to 99.7%. 21 Positive screening results may be found to be false upon follow-up investigation involving additional scans or lung biopsy. To mitigate harm and maximise benefit, screening has been limited to high risk individuals based on their age and smoking history, using risk prediction modelling.22,23
The United States (USA) have the longest-running lung cancer screening programmes. Participation rates have been low, at 14% of eligible individuals, 24 and rates tend to be even lower among groups at highest risk, including racially minoritised groups,25,26 those with low socioeconomic status, 26 and current smokers. 27 Reasons for low uptake include lack of access to lung cancer screening and treatment, 28 low awareness and education about lung cancer screening,28,29 and uneven programme implementation. 30 Other evidence points to the importance of how people perceive screening benefits and harms, 28 but there is a lack of understanding of how those targeted for lung cancer screening value this intervention and what factors they consider when making decisions about whether or not to take up screening. Such understanding will be important to inform the development of screening programmes. This study aimed to contribute to filling this gap by conducting a review of patient and public perspectives on the benefits and harms of lung cancer screening with LDCT.
Methods
We conducted a mixed methods systematic review and integrative synthesis, using a convergent integrated mixed methods design.31–33 We collected quantitative data from quantitative and mixed methods studies, and qualitative data from qualitative and mixed methods studies, and integrated these using a narrative approach. 34 The study protocol was published on PROSPERO. 35
Search strategy
We searched for original studies in any global jurisdiction published between 1 January 2002 and 6 October 2022 using six databases: MEDLINE, Cumulated Index to Nursing and Allied Health Literature (CINAHL), Embase, Emcare, Scopus, and Social Science Citation Index (SSCI). The search strategy was developed with a medical librarian (CH) and topic experts (MP, PD). Search terms for lung cancer screening were combined with search strings for qualitative and quantitative research using validated search filters (Online Supplement Table S1).36,37 The search was first conducted in MEDLINE and then adapted using keywords and syntax specific to the remaining databases. A search validation exercise was conducted by identifying five known articles prior to the search and looking for their inclusion in the MEDLINE search results. Records from all databases were consolidated and duplicates removed. Remaining records were screened for eligibility.
Study eligibility
Two reviewers (MP and one of AC, KS, or MC) independently screened titles and abstracts for eligibility according to a set of inclusion and exclusion criteria established a priori (Online Supplement Table S2). Studies were included that explored knowledge, attitudes, beliefs, perceptions, perspectives, opinions, judgements, and preferences regarding the benefits and harms of lung cancer screening with LDCT. Studies reporting on facilitators of and barriers to screening were included if they documented public perspectives on screening benefits and harms. Benefits and harms were conceptualised as individual benefits or harms rather than population-level or system-wide benefits or harms.
Full-text articles of eligible titles and abstracts were retrieved and independently screened for eligibility (MP and one of AC, KS, or MC). Discrepancies were resolved via consensus between MP and one of AC, KS, or MC. We calculated interrater reliability for title and abstract screening and full-text screening using percentage agreement and estimated with the Cohen’s Kappa statistic (Online Supplement Table S3).
Data extraction
One reviewer (MP) extracted quantitative and qualitative study data; data extraction was reviewed for completeness and accuracy by a second reviewer (AC, KS, or MC). Extracted data described benefits or harms as identified by the study author or our author team. We considered physical, psychological, social, financial, and other reported benefits and harms. For quantitative studies, we extracted and tabulated outcomes and measurements, and any related tests of statistical significance for between-group comparisons by intervention (e.g., pre-post), socioeconomic status, racialised or ethnic group, and smoking status (Online Supplement Table S4). For qualitative studies, we extracted results and interpretations of findings reported in included studies. Qualitative data were coded as outcomes using NVivo software (QSR International). Codes were directly copied from or stayed close to the results categories, themes or ideas as reported by authors.
Data analysis and synthesis
Analytic framework.
Quality assessment
Two reviewers (MP and AC) independently evaluated study quality using the Mixed Methods Appraisal Tool (MMAT). 39 The MMAT considers key quality domains associated with each of the five study designs included in this review. Quality assessment was conducted to contextualise the strength of study findings 40 ; it did not affect study inclusion or interpretation. Differences between reviewers’ quality assessments were resolved by discussion leading to consensus between MP and one of AC, KS, or MC.
Reporting
We followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) 2020 reporting checklist (Online Supplement Table S6). 41
Results
Included studies and participants
Database searches yielded 10,038 records after duplicates were removed. After title and abstract screening, 176 full-text articles were screened for eligibility, resulting in 49 unique studies for inclusion (Figure 1). The review considered 20,120 participants in 26 quantitative, 18 qualitative, and 5 mixed methods studies (Table 2). Most participants (81%) were in 18 quantitative descriptive studies (Table 3). Qualitative studies frequently used semi-structured individual interviews and focus groups, while quantitative studies mostly used surveys to collect data. Thirty-seven studies representing 42% of participants were conducted in the USA (Table 2). Participants were mostly white (11,647 participants in 28 studies); half of participants were current smokers. PRISMA flow chart. Characteristics of participants from included studies. aNumber of people in the lowest socioeconomic status category from each study. bNumber of people in the largest race or ethnicity category from each study. Methodologies used by included studies.
Quality assessment
Study quality was considered acceptable (Online Supplement Table S7). Qualitative studies rarely reported study methodology; it was therefore not possible to determine the appropriateness of the approach to answer the research question (MMAT question 1.1). Most quantitative studies were descriptive and found to be of acceptable quality. There was a lack of detailed information about randomisation and blinding methods for randomised controlled trials. Participant representativeness was a concern for some quantitative non-randomised studies due to high and unexplained non-response rates. Integration was a concern for some mixed methods studies.
In the following, we report the main findings in line with our analytical framework (Table 1). This review identified 49 included papers, with an overview of key characteristics of included studies shown in Online Supplement Table S8, and related references included in Online Supplement S9 and cited as S1 to S48.
Overall perspectives
Overall, participants had positive perspectives on lung cancer screening with LDCT. There was wide acceptance of lung cancer screening as a tool for early detection and treatment similar to screening programmes for other cancers S1–S3 that could also reduce anxiety about cancer. S4 Some participants who believed strongly in the benefits of screening thought that eligibility should be expanded S3 and that it should be offered widely at no cost. S5 A small number of participants believed screening was unnecessary, of low benefit, and a waste of time, effort, and expense. S6–S8
There appeared to be a general sense that the benefits of early detection outweighed potential harms, S9,S10 and this was independent of people’s eligibility for and/or participation in lung cancer screening, S11,S12 as well as engagement with educational and decision aid interventions. S11,S13,S14 Study participants appeared to trust that the offer of screening implied its overall benefit and little likelihood of harm. Some considered screening to be a prudent precautionary measure to “be safe not sorry”. S15 p8
Harms were either not recognised (“why would there be cons?”) S15 p8,S9,S16 or acknowledged and rationalised by early detection benefits. Concerns about radiation exposure were seen to be outweighed by the low dose of CT. Harms related to screening accuracy were considered unavoidable, but not as readily justified as radiation exposure. Some expressed a desire for further health intervention, including follow-up investigation of suspicious findings. S9,S15–S19 Others were less confident in screening and the potential for personal benefit. This view was particularly prevalent among African Americans who were current smokers, S12,S14,S15,S17 and among people from deprived backgrounds and current smokers. S20,S21 Participants in several studies wanted to assess benefits and harms for themselves. S6,S14,S22,S23
Physical benefits
Participants in most studies viewed screening as a tool for the early detection and treatment of lung cancer S1–S3,S8,S9,S11,S13,S15,S19,S23–S34 that could reduce the risk of dying from lung cancer. S1,S2,S10–123,S15,S19,S20,S27,S31,S35–S39 People who previously smoked tobacco, those of higher economic status as well as white participants more often believed in the benefits of early detection, were willing to be screened and have lung cancer treatment, and thought that there was a good chance of surviving with screen-detected lung cancer. S20,S21,S40–S42 Current smokers considered screening as the medical community doing something helpful for them. S88,S9,S32 Some current smokers did not think that they would get lung cancer even if screening detected an abnormal growth on the lung. S5 They also believed that current smokers who had lung cancer symptoms, were heavy smokers or were exposed to occupational or environmental lung carcinogens, needed screening more than themselves. S3,S5
Psychological benefits
Screening was seen as an opportunity to gain knowledge about lung health, S1–S3,S10,S12,S13 and on important components of the lung screening pathway, from incidental findings to overdiagnosis and invasive follow-up procedures. S10 Screening was seen to reduce uncertainty and anxiety about lung health status by providing a negative or actionable positive screening result, S4,S6,S18,S21–S23,S33,S34 and, thus, reassurance for oneself or their family when given a negative screening result. S5,S11,S12,S14,S21,S23,S27,S31,S37,S43 Screening results were seen as a means to decide whether or not to quit smoking: negative screening results provided relief S5,S10 and a motivation to quit S14,S21,S27,S37,S43 or continue smoking until screening showed evidence of lung cancer. S12,S14
There was a view that LDCT could provide definitive information about the presence, absence, and future risk of developing lung cancer. S5,S11,S16 Current and former smokers who were concerned about the degree of lung damage caused by smoking saw screening as a means to have certainty or satisfy curiosity, S3,S5,S32 although some recognised that screening results are not certain S22 and they wanted to reduce uncertainty through additional investigation of positive screening findings. S10 Incidental findings and false positives were perceived as a relief by some, reflecting greater worry about cancer compared to other lung diseases. S10 Even where late-stage lung cancer was detected upon screening, participants stated that this could help them prepare their personal affairs and gain additional time with their family. S21,S23
Studies reported instances of knowledge avoidance among people who expected a late-stage diagnosis, had difficulties accessing screening, felt smoking-related stigma, held smoking-related fatalistic beliefs, or minimised smoking-related health risks. S3,S22 Participants stated that they would be reassured by screening programmes that provide clear explanations about the screening invitation and procedures, and that engage supportive networks of family, friends and health providers in the screening process. S15,S44
Physical harms
Screening errors and radiation exposure were considered intrinsic to screening S19 and seen to be generally acceptable given the benefits of early detection. S1–S3,S10,S14,S15,S19,S24–S26,S30,S35,S36,S43–S45 Study participants thought that screening accuracy was important S1,S2,S12,S27,S28,S40,S41 and that LDCT was accurate. S23,S46 There were concerns about the risks of false positive S7,S10,S14,S19,S34 and false negative S19 screening results, as well as the possibility for misdiagnosis, S34 overdiagnosis, S10,S15,S22 and overtreatment. S15,S18
Some participants were hesitant about screening when they learned about the likelihood of a false positive result. S7,S10,S14,S15,S18,S19 Avoiding false positive results, biopsy, and follow-up investigation was more important for low compared to high income participants S36 with mixed findings for Latino populations. S36,S46 Participants were more worried about false negative than false positive screening results. S19 They were moderately concerned S24,S25,S30,S35 and confused about the concept of overdiagnosis. S10,S19,S22 Overdiagnosis was considered a benefit for participants who considered the risk of not treating an indolent cancer with indeterminate prognosis S10,S19 and a harm due to the life-changing effects of being diagnosed with lung cancer and potential impacts on future lung health. S10 Overtreatment was considered a harm. S10,S15,S18 One participant stated not wanting to be treated for “something that I haven’t even got”. 15 p6
There was low to moderate concern about screening-related radiation exposure. S11,S14,S24–S27,S29–S31,S37,S43,S46,S47 Radiation exposure from a single scan was generally accepted but there were concerns about possible harms from multiple scans. S21,S23 Participants were unclear about the dose of radiation used in LDCT and potential side effects S6,S23 but they trusted that physicians use a safe dose of radiation. S4 Worries about physical discomfort or pain during lung cancer screening S13,S27,S29,S37,S46 were related to machine enclosure S3,S33 and uncertainty about the use of contrast dye S32 among participants who had no previous experience of computerised tomography. S18
Psychological harms
Study participants reported fear and anxiety in relation to both the process and possible outcomes of screening, in particular being diagnosed with lung cancer S3,S6–S8,S11–S13,S21,S27,S32–S34 and about having abnormal CT results. S11,S13–S15,S43 There were also concerns about false positive results, S10,S15 incidental findings, S15 follow-up investigation, S15 and lung cancer treatment. Compared to non- or former smokers, current smokers tended to be more concerned about lung cancer diagnosis, indeterminate nodules,S19 what screening would reveal about their lung health due to smoking and other health risk behaviours, S7,S8,S18,S21 and the treatment consequences for each of these possible outcomes. S4,S7,S21,S25 Fear of having lung cancer was influenced by experiences of a family member or friend having died of lung cancer. S3,S4,S6,S16,S21,S34 Current smokers noted that they would rather not pursue screening to avoid learning about their lung health. S3,S7,S21,S32,S33
Invitation to screening and interaction with physicians caused anxiety. S3,S21 Waiting for screening and follow-up results was described as protracted and unpredictable; a “worrying time”. S3,S15,S23 p6 These issues were of lower concern for participants with prior experience of waiting for CT results, who had positive views about screening S23 and the benefits of early detection. S16
There was a view, especially among current and former smokers, that lung cancer risk factors other than smoking warranted greater attention from doctors S3,S5,S14 and that screening invitations should be worded to not single out people with a history of smoking. S21 They also expressed concerns about blame and discrimination given the association between smoking and lung cancer, S1,S2,S11,S14,S21 which would deter some from discussing screening with their physician, S32 especially with those who “don’t know the culture we grew up in”: S48 p65 “I think that if you’re a smoker or an ex-smoker a lot of doctors treat you like you’re a leper. It’s a dirty disease because you smoke.” S3 p168 In one study, Chinese Americans described wanting screening where they could not be personally identified because this would help to preserve their good public image. S32
Current smokers tended to expect that screening would identify lung cancer and perceived the benefits of screening, and of lung cancer treatment effectiveness, to be low, and frequently held fatalistic beliefs about lung cancer. This view tended to be common among older smokers, who expected a low tolerance of lung cancer treatment and poor survival probability compared to younger smokers. S16,S21 Some current smokers reported being tired of repeated reminders about smoking cessation, S15 seeing this as a deterrent to participating in screening. S21
Financial and opportunity costs
Costs associated with screening, potential follow-up investigation, and treatment was seen as an important factor influencing decisions of whether to participate in lung cancer screening, S1,S2,S6–S8,S18,S32,S34 and this was highlighted by at least 70% of participants in reviewed studies. S12,S28 Financial concerns were raised in relation to insurance status, especially among current smokers, S6–S8,S11,S18,S27,S32,S34,S41,S46 with concerns about accessibility of screening in terms of distance and time requirements raised in studies in the USA (9 studies) and Australia (1 study), S3,S7,S11,S18,S26,S27,S31,S32,S34,S46 and among low-income rural residents, S6 current and former smokers, S41 and, in the USA, non-Latinos. S46 People with health problems that required ongoing care reported that screening could place an additional burden on their time. S4,S33 There was a generally expressed need for greater geographic availability of and daily appointments for screening, S3,S34 as well as employer support for time off work, and family help with travel to a screening centre. S23
Discussion
This review of public perceptions of the benefits and harms of screening for lung cancer with LDCT found generally positive views. Most participants in reviewed studies valued the benefits of early detection, diagnosis, and treatment given a true positive screening result. They also valued reassurance from a true negative screening result. These perceived personal benefits were seen to outweigh risks associated with screening error and radiation exposure risks, which were seen as rare and inherent screening harms.
Perceptions varied by subgroups at higher risk of lung cancer, such as current smokers, who highlighted a tension between wanting to know about their lung health while at the same avoiding this knowledge; this was mainly driven by concerns about stigma and blame, fear and anxiety about being diagnosed with lung cancer, and fatalistic beliefs about lung cancer. Costs associated with screening, whether actual or perceived, posed a particular challenge for people with low incomes and these concerns could not easily be overcome by their otherwise positive views on early detection benefits. Thirteen studies focused on racialised populations with variable perspectives on screening that may be mediated by smoking and socioeconomic status.
Individual and public health dimensions of screening benefits and harms
Participants in reviewed studies tended to assess screening to be personally beneficial and rationalised screening harms by the potential for early detection and reassurance. Populations targeted for cancer screening frequently hold favourable views that emphasise benefits and minimise harms. 42 We found that participants had pro-screening attitudes because of their desire for reassurance and gaining personal health information. 43
Lung cancer screening is a public health and health care intervention. 44 The main benefit is reduced lung cancer mortality observable at the population level. However, there are harms and it is difficult for potential screening participants to understand that they are unlikely to personally benefit from screening even if they are at high risk for lung cancer. As lung cancer screening evolves, it remains crucial that screening programmes effectively communicate balanced evidence about benefits and harms and engage with people’s values, expectations, and lived experiences in decision-making. 45
Strengths and limitations
A main strength of this review was the inclusion of quantitative, qualitative, and mixed methods primary studies from a robust search of the lung cancer screening literature. Convergent integration of evidence from methodologically diverse studies created a rich and nuanced narrative. There was a lack of studies of public perceptions in countries that conduct research in or have introduced lung cancer screening activities; this may be because we only included studies published in English language. Study quality was limited by incomplete methods reporting in included studies. Studies also varied in how lung cancer screening benefits and harms were conceptualised and evaluated, with a wide range of outcomes that prevented aggregate outcome assessment across many studies using meta-analysis or other forms of quantitative synthesis. Meta-synthesis of qualitative study findings was similarly challenging because of variability in studies while at the same time illustrating the breadth of views on different types of benefits and harms. Public perceptions research that includes a wider range of relevant perspectives may enrich our understanding of benefits and harms that can contribute to improved lung cancer screening policy and clinical decision-making.
Implications for policy and research
We found that the public, especially current smokers, had serious concerns about the potential psychological harms of screening. Stigma, fear, and anxiety may partly explain low participation rates. 46 Efforts to increase screening access are being made 47 and will require detailed ethical and policy deliberation about the distribution of potential screening benefits and harms and inequities along the lung cancer screening pathway. 48 Policymakers can play an important role in helping to destigmatise screening, reduce the risks of screening-related psychological harm, and address unmet primary and lung cancer care needs.
There is need for further research on public perceptions of lung cancer screening among populations at higher risk for lung cancer, in particular racialised communities and populations in Asian, South American, and African regions. Studies should seek to also understand views on primary prevention of lung cancer. There is a need for greater understanding of the social and political determinants of lung cancer and the values of equity-denied, oppressed, and marginalised populations to help inform appropriate policy action.
Supplemental Material
Supplemental Material - Public perspectives on the benefits and harms of lung cancer screening: A systematic review and mixed-method integrative synthesis
Supplemental Material for Public perspectives on the benefits and harms of lung cancer screening: A systematic review and mixed-method integrative synthesis by Manisha Pahwa, Alexandra Cernat, Julia Abelson, Paul A Demers, Lisa Schwartz, Katrina Shen, Mehreen Chowdhury, Caroline Higgins and Meredith Vanstone in Journal of Health Services Research & Policy.
Footnotes
Acknowledgments
The authors would like to acknowledge research librarians at the Health Sciences Library at McMaster University who supported the development of the health database search strategy.
Declaration of conflicting interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This research was supported by training awards received by MP under the primary supervision of MV from the Ontario Graduate Scholarship and the Canadian Institutes of Health Research Frederick Banting and Charles Best Canada Graduate Scholarships Doctoral Research Award (#434441). AC’s contributions were also supported by a training award received under the primary supervision of MV from the Canadian Institutes of Health Research Vanier Canada Graduate Scholarships. MV is Canada Research Chair in Ethical Complexity in Primary Care. Funding agencies did not influence this review.
Ethical statement
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References
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