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Multilevel Opportunities to Address Lung Cancer Stigma across the Cancer Control Continuum

Open ArchivePublished:May 22, 2018DOI:https://doi.org/10.1016/j.jtho.2018.05.014

      Abstract

      The public health imperative to reduce the burden of lung cancer has seen unprecedented progress in recent years. Fully realizing the advances in lung cancer treatment and control requires attention to potential barriers in their momentum and implementation. In this analysis, we present and evaluate the argument that stigma is a highly significant barrier to fulfilling the clinical promise of advanced care and reduced lung cancer burden. This evaluation of the stigma of lung cancer is based on a multilevel perspective that incorporates the individual, persons in the individual's immediate environment, the health care system, and the larger societal structure that shapes perceptions and decisions. We also consider current interventions and interventional needs within and across aspects of the lung cancer continuum, including prevention, screening, diagnosis, treatment, and survivorship. Current evidence suggests that stigma detrimentally affects psychosocial, communication, and behavioral outcomes over the entire lung cancer control continuum and across multiple levels. Interventional efforts to alleviate stigma in the context of lung cancer show promise, yet more work is needed to evaluate their impact. Understanding and addressing the multilevel role of stigma is a crucial area for future study to realize the full benefits offered by lung cancer prevention, control, and treatment. Coordinated, interdisciplinary, and well-conceptualized efforts have the potential to reduce the barrier of stigma in the context of lung cancer and facilitate demonstrable improvements in clinical care and quality of life.

      Keywords

      Introduction

      Recent advances in prevention, screening, treatment, and management of symptoms have brought the promise of decreased lung cancer burden closer to reality.
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      Low-dose computed tomography (LDCT) screening has demonstrated effectiveness in increasing early detection of localized, resectable thoracic tumors.
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      Screening for lung cancer with low-dose computed tomography: a systematic review to update the U.S. Preventive Services Task Force recommendation.
      Molecular testing now facilitates targeting and personalization of treatment and is increasingly being integrated into standard clinical practice. After decades of effort, immune checkpoint inhibitors have demonstrated promising results and have received U.S. Food and Drug Administration approval for treatment of metastatic NSCLC.
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      Pembrolizumab plus chemotherapy in metastatic non–small-cell lung cancer.
      Simultaneously, a growing global community of lung cancer advocates are highlighting survivorship stories, promoting research and evidence-based care, and focusing on policy needs.

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      Despite these promising advances across many aspects of lung cancer care and control, low clinician adoption, limited patient uptake, and other implementation challenges have been observed.
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      Lung cancer screening with low-dose computed tomography in the United States-2010 to 2015.
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      Access to cancer specialist care and treatment in patients with advanced stage lung cancer.
      Therefore, to fully realize the impact of the research and clinical advances, it is important to understand and address significant modifiable barriers to their successful implementation. In this article, we present and provide evidence supporting the argument that the stigma of lung cancer (the experience and internalization of negative appraisal and devaluation from others
      • Hamann H.A.
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      Stigma among patients with lung cancer: a patient-reported measurement model.
      ) is a formidable barrier to fulfilling the clinical promise of high-quality care and reduced lung cancer burden. In addition to documenting the impact of lung cancer stigma, we focus on promising interventions and future research directions to address this stigma and improve the outcomes of lung cancer care.
      Attention to the robust causal connection between smoking and lung cancer, although crucial for tobacco control, may have unintended consequences that generate blaming responses and biased negative perceptions toward patients with lung cancer and those at high risk for lung cancer (e.g., current smokers).
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      Tobacco control, stigma, and public health: rethinking the relations.
      Our previous work has identified three primary elements of lung cancer stigma from the patient's perspective: (1) perceived stigma (how what others think and say is evaluated by the patient); (2) internalized stigma (how perceived stigma can affect patients through self-blame and guilt); and (3) constrained disclosure (how stigma limits discussions of lung cancer with others).

      Hamann HA, Shen MJ, Thomas AJ, Lee SJC, Ostroff JS. Development and preliminary psychometric evaluation of a patient-reported outcome measure for lung cancer stigma: the lung cancer stigma inventory (LCSI) [e-pub head of print]. Stigma and Health. http://dx.doi.org/10.1037/sah0000089. Accessed June 27, 2018.

      For many patients who are at high risk of or have received a diagnosis of lung cancer, the stigma can detrimentally affect willingness to engage in screening for early detection, cause patients to delay seeking medical evaluation for presenting symptoms, and limit their involvement in lung cancer treatment and survivorship care.
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      • et al.
      A systematic review of the impact of stigma and nihilism on lung cancer outcomes.
      • Carter-Harris L.
      Lung cancer stigma as a barrier to medical help-seeking behavior: practice implications.
      Although there may be subtle positive effects of stigma that foster advocacy and social cohesion for some patients,
      • Hamann H.A.
      • Ostroff J.S.
      • Marks E.G.
      • Gerber D.E.
      • Schiller J.H.
      • Lee S.J.C.
      Stigma among patients with lung cancer: a patient-reported measurement model.
      most investigations have reported on the pervasive negative consequences of lung cancer stigma. Lung cancer stigma can have far-reaching deleterious effects that range from reduced involvement in prevention and early detection interventions, negative psychosocial impact, impaired patient-clinician communication, inadequate access to diagnosis and treatment, and limited funding and public support for lung cancer research and care. Developing and testing interventions to ameliorate lung cancer stigma requires comprehensive understanding of mechanisms and targeted approaches across the cancer care continuum.
      To understand the full scope and impact of lung cancer stigma, a multilevel framework is needed. The multilevel perspective incorporates the individual (patient), persons in the patient's immediate environment (e.g., family, friends), persons in the health care system (e.g., oncologic and primary care providers), and the larger societal structure that shapes perceptions and decisions (e.g., public attitudes, policy, media campaigns, research funding). Stigma is largely social in nature in that it is commonly perceived and internalized with an interpersonally and behaviorally relevant impact. Socioecological system models
      • Brofenbrenner U.
      Toward an experimental ecology of human development.
      provide useful frameworks to understand multilevel processes and address connections both within and across levels (Fig. 1). Within this model, interventions to improve one level (e.g., interpersonal communication) can also improve outcomes at other levels (e.g., individual quality of life).
      • Cook J.E.
      • Purdie-Vaughns V.
      • Meyer I.H.
      • Busch J.T.A.
      Intervening within and across levels: a multilevel approach to stigma and public health.
      Figure thumbnail gr1
      Figure 1Socioecological model to understand multilevel processes of lung cancer stigma. In the context of lung cancer stigma, the intrapersonal level centers on thoughts, feelings, and actions of the affected person. The interpersonal level centers on the social relationships and perceptions of others. The societal level addresses social conditions, structural components, and public attitudes. Adapted from Bronfenbrenner
      • Brofenbrenner U.
      Toward an experimental ecology of human development.
      and Cook et al
      • Cook J.E.
      • Purdie-Vaughns V.
      • Meyer I.H.
      • Busch J.T.A.
      Intervening within and across levels: a multilevel approach to stigma and public health.
      with permission from Elsevier.
      A second important consideration of lung cancer stigma is its impact across the entire continuum of care and control, including prevention (e.g., smoking cessation interventions), screening and early detection, diagnosis, treatment, and survivorship (Fig. 2).
      • Rowland J.H.
      • Bellizzi K.M.
      Cancer survivors and survivorship research: a reflection on today's successes and tomorrow's challenges.
      At each phase of the continuum, lung cancer stigma may be a barrier to the successful implementation of research advances to reduce the lung cancer burden. Therefore, it is crucial that interventions focused on stigma consider relevant patient and quality of care outcomes across the lung cancer care continuum. This review addresses our current understanding of lung cancer stigma within these multilevel and cancer continuum perspectives. Although we focus primarily on lung cancer care within the United States, we have aimed to summarize the literature and perspectives on stigma from around the world when possible. In particular, we have focused on the status of current interventions and interventional needs within and across levels and experiences in the cancer continuum. Organizing our understanding of lung cancer stigma within this multilevel, multiphase framework allows for the development of a road map to reduce inequities affecting patients with lung cancer
      • Lathan C.S.
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      and promote efficient and effective implementation of innovations in delivery of lung cancer care.
      Figure thumbnail gr2
      Figure 2Continuum of cancer care. The stages of the cancer continuum include prevention, detection, diagnosis, treatment, and survivorship. At each stage of the continuum, the stigma of lung cancer may be a barrier to the successful application of research advances to reduce the burden of lung cancer. Therefore, it is crucial that interventions focused on stigma acknowledge and address each element of this extended lung cancer care continuum. Reprinted with permission from J.H. Rowland.
      • Rowland J.H.
      • Bellizzi K.M.
      Cancer survivors and survivorship research: a reflection on today's successes and tomorrow's challenges.

      An Intrapersonal (Individual) Perspective to Addressing Lung Cancer Stigma

      An intrapersonal perspective in the context of lung cancer stigma emphasizes the thoughts, feelings, and actions of the affected individual
      • Cook J.E.
      • Purdie-Vaughns V.
      • Meyer I.H.
      • Busch J.T.A.
      Intervening within and across levels: a multilevel approach to stigma and public health.
      (see Fig. 1). Assessing the impact of lung cancer stigma at the intrapersonal level involves consideration of the patient’s psychosocial (e.g., depression, distress, self-esteem) and behavioral (e.g., screening participation, treatment adherence) processes likely influenced by public perception and internalization of stigma.
      • Cook J.E.
      • Purdie-Vaughns V.
      • Meyer I.H.
      • Busch J.T.A.
      Intervening within and across levels: a multilevel approach to stigma and public health.

      Prevention

      Rates of smoking in both adults and youths in the United States have been near an all-time low since the popularization of smoking in the 1940s. In the 50 years since the 1964 Surgeon General’s report Smoking and Health, rates of smoking among U.S. adults have fallen from a high of 43% to a national low of 15.5%.

      US National Center for Chronic Disease Prevention and Health Promotion Office on Smoking and Health. The health consequences of smoking—50 years of progress. http://www.ncbi.nlm.nih.gov/pubmed/24455788. Accessed February 28, 2018.

      In 2016, only 8% of high school students smoked cigarettes.
      • Jamal A.
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      • et al.
      Tobacco use among middle and high school students—United States, 2011–2016.
      Unfortunately, these gains in tobacco control have not benefited all individuals equally, such that the rate of cigarette smoking remains high among individuals with low income and education, certain racial and ethnic minorities, those with serious mental illness, those with physical disabilities, sexual and gender minorities, residents of rural communities, and other vulnerable subpopulations.

      National Cancer Institute. A socioecological approach to addressing tobacco-related health disparities. https://cancercontrol.cancer.gov/brp/tcrb/monographs/22/docs/m22_complete.pdf. Accessed February 28, 2018.

      Not only have some communities not benefited as substantially as others but aggressive tobacco control messages may also be engendering harm as an unintended consequence, reducing empathy for dependent tobacco users, and creating an oppositional and contentious environment between tobacco users and non–tobacco users.
      • Stuber J.
      • Galea S.
      • Link B.G.
      Smoking and the emergence of a stigmatized social status.
      Current disparities in smoking prevalence, particularly among various subpopulations, are likely contributing to the declining social acceptance and stigmatization of current smoking. The tobacco industry’s practice of targeting marketing to certain racial and ethnic groups is thought to further contribute to social discrimination and stigmatization of smokers.

      National Cancer Institute. A socioecological approach to addressing tobacco-related health disparities. https://cancercontrol.cancer.gov/brp/tcrb/monographs/22/docs/m22_complete.pdf. Accessed February 28, 2018.

      International evidence suggests that smokers’ perceived and internalized stigma is universal and that it not only has a negative impact on mood and self-esteem but also might inhibit smoking cessation efforts through concealment and social withdrawal.
      • Bayer R.
      • Stuber J.
      Tobacco control, stigma, and public health: rethinking the relations.
      • Stuber J.
      • Galea S.
      • Link B.G.
      Smoking and the emergence of a stigmatized social status.
      • Siahpush M.
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      • Fong G.T.
      Socioeconomic variations in nicotine dependence, self-efficacy, and intention to quit across four countries: findings from the International Tobacco Control (ITC) Four Country Survey.

      Thompson L, Pearce J, Barnett JR. Moralising geographies: stigma, smoking islands and responsible subjects. Area. 39:508–517.

      • Evans-Polce R.J.
      • Castaldelli-Maia J.M.
      • Schomerus G.
      • Evans-Lacko S.E.
      The downside of tobacco control? Smoking and self-stigma: a systematic review.
      • Stuber J.
      • Galea S.
      Who conceals their smoking status from their health care provider?.
      Smokers often report self-blame, guilt, and awareness of their marginalization as smokers. In a recent intervention trial, low-income smokers who reported higher levels of baseline stigma were less likely to engage in a smoking cessation intervention.
      • Hammett P.
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      • Nelson D.
      • et al.
      A proactive smoking cessation intervention for socioeconomically disadvantaged smokers: the role of smoking-related stigma.
      Stigma has been associated with misreporting of smoking status to health care providers, particularly in hospitalized smokers and those with chronic medical conditions.
      • Stuber J.
      • Galea S.
      Who conceals their smoking status from their health care provider?.
      • Pell J.
      • Haw S.
      • Cobbe S.
      • et al.
      Validity of self-reported smoking status: comparison of patients admitted to hospital with acute coronary syndrome and the general population.
      These findings highlight the importance of gaining a greater understanding of the role of stigma as a barrier for smoking cessation, including a focus on tailoring cessation interventions to optimize engagement and cessation outcomes.

      Screening

      In the context of lung cancer screening, evidence suggests that stigma is a powerful barrier to effective early detection with LDCT of the chest.
      • Carter-Harris L.
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      • Hanna N.
      • Rawl S.M.
      Lung cancer screening: what do long-term smokers know and believe?.
      Compared with uptake of other types of cancer screening at the same implementation stage, the rate of LDCT screening of eligible patients remains very low (approximately 4%).
      • Jemal A.
      • Fedewa S.A.
      Lung cancer screening with low-dose computed tomography in the United States-2010 to 2015.
      • Doria-Rose V.P.
      • White M.C.
      • Klabunde C.N.
      • et al.
      Use of lung cancer screening tests in the United States: results from the 2010 National Health Interview Survey.
      Of equal importance is the fact that only 10% of screening-eligible patients have engaged in a discussion about the option of screening with their health care clinician.
      • Carter-Harris L.
      • Tan A.S.L.
      • Salloum R.G.
      • Young-Wolff K.C.
      Patient-provider discussions about lung cancer screening pre- and post-guidelines: Health Information National Trends Survey (HINTS).
      In qualitative interviews of screening-eligible individuals, Carter-Harris et al.
      • Carter-Harris L.
      • Ceppa D.P.
      • Hanna N.
      • Rawl S.M.
      Lung cancer screening: what do long-term smokers know and believe?.
      identified patient-reported stigma as a significant hindrance to lung cancer screening; patients described concerns about being judged and blamed by health care clinicians as limiting their engaging in screening. In terms of intrapersonal interventions, recent work has focused on developing patient-focused lung cancer screening decision aids,
      • Volk R.J.
      • Linder S.K.
      • Leal V.B.
      • et al.
      Feasibility of a patient decision aid about lung cancer screening with low-dose computed tomography.
      • Lau Y.K.
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      • Cao P.
      • et al.
      Evaluation of a personalized, web-based decision aid for lung cancer screening.
      including those that address the role of stigma.
      • Carter-Harris L.
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      • Goyal A.
      • et al.
      Development and usability testing of a computer-tailored decision support tool for lung cancer screening: study protocol.
      In particular, tailoring screening messages by smoking status has the potential to decrease stigma in former smokers who are eligible for lung cancer screening and are engaging with such a decision aid.
      • Carter-Harris L.
      • Comer R.S.
      • Goyal A.
      • et al.
      Development and usability testing of a computer-tailored decision support tool for lung cancer screening: study protocol.
      Although more work is needed, targeted empathic messages and tailored decision aids hold the promise to reduce stigma and increase informed uptake of lung cancer screening.

      Diagnosis and Treatment

      Stigma-related fears are associated with patient-initiated delays in seeking medical help that may result in more late-stage diagnoses.
      • Carter-Harris L.
      Lung cancer stigma as a barrier to medical help-seeking behavior: practice implications.
      • Tod A.M.
      • Craven J.
      • Allmark P.
      Diagnostic delay in lung cancer: a qualitative study.
      Early screening and recognition of lung cancer symptoms combined with timely medical help–seeking behavior can facilitate earlier-stage diagnoses and increased survival; however, too few lung cancer diagnoses are made in these early stages.
      • Wender R.
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      • Barrera E.
      • et al.
      American Cancer Society Lung Cancer Screening Guidelines.
      A cross-sectional, quantitative study reported significant associations between patient-reported stigma and increased time from onset of symptoms to medical help seeking.
      • Carter-Harris L.
      Lung cancer stigma as a barrier to medical help-seeking behavior: practice implications.
      Other qualitative reports
      • Tod A.M.
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      Diagnostic delay in lung cancer: a qualitative study.
      • Corner J.
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      Experience of health changes and reasons for delay in seeking care: a UK study of the months prior to the diagnosis of lung cancer.
      • Carter-Harris L.
      • Hermann C.P.
      • Draucker C.B.
      Pathways to a lung cancer diagnosis.
      • Crane M.
      • Scott N.
      • O’Hara B.J.
      • et al.
      Knowledge of the signs and symptoms and risk factors of lung cancer in Australia: mixed methods study.
      have supported this theme, noting a reluctance of patients to seek medical care for symptoms owing to fear of being blamed by their clinicians. Results suggest that efforts aimed to educate patients about lung cancer symptoms should also address the role of stigma as a barrier to earlier diagnosis. Reducing stigma in this context could have powerful effects on symptom recognition, earlier diagnosis, and enhanced survival outcomes.
      An expanding research base has also addressed the psychosocial and behavioral intrapersonal impact of stigma in the context of treatment. Despite advances in targeted therapies, a significant percentage of patients with lung cancer do not receive molecular testing and evidence-based anticancer treatment,
      • Ganti A.K.
      • Hirsch F.R.
      • Wynes M.W.
      • et al.
      Access to cancer specialist care and treatment in patients with advanced stage lung cancer.
      • Lim C.
      • Tsao M.S.
      • Le L.W.
      • et al.
      Biomarker testing and time to treatment decision in patients with advanced nonsmall-cell lung cancer.
      • Gutierrez M.E.
      • Choi K.
      • Lanman R.B.
      • et al.
      Genomic profiling of advanced non–small cell lung cancer in community settings: gaps and opportunities.
      and they are less likely to engage in clinical trials,
      • Murthy V.H.
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      • Gross C.P.
      Participation in cancer clinical trials.
      participate in supportive care,
      • Kumar P.
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      • Corcoran A.
      • et al.
      Utilization of supportive and palliative care services among oncology outpatients at one academic cancer center: determinants of use and barriers to access.
      • Yates P.
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      • Zhao I.
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      Supportive and palliative care for lung cancer patients.
      and seek rehabilitation services
      • Cheville A.L.
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      • Flores A.M.
      How receptive are patients with late stage cancer to rehabilitation services and what are the sources of their resistance?.
      despite high levels of distress and comparatively poor quality of life. Again, the role of patient-reported stigma in limited engagement and adherence to treatment is potentially significant. In a cross-sectional quantitative study of 231 patients with lung cancer, stigma was significantly associated with reduced patient-reported engagement in care.

      Price SN, Ostroff JS, Shen M, Thomas AJ, Lee SJC, Hamann HA. Advocacy and stigma among patients with lung cancer. Paper presented at: 38th Annual Meeting of the Society of Behavioral Medicine. March 29–April 1, 2017; San Diego, CA.

      Hamann HA, Borderud S, Higashi R, et al. Association between stigma, patient activation and patient-provider communication in lung cancer care. Paper presented at: 36th Annual Meeting of the Society of Behavioral Medicine. April 22–25, 2015; San Antonio, TX.

      In a qualitative study of 65 individuals with lung cancer, a salient theme involved highly stigmatized patients who questioned whether they deserved treatment and were less likely to seek out information about treatment options.
      • Hamann H.A.
      • Ostroff J.S.
      • Marks E.G.
      • Gerber D.E.
      • Schiller J.H.
      • Lee S.J.C.
      Stigma among patients with lung cancer: a patient-reported measurement model.
      More research is needed to untangle the complex relationships between engagement in care, treatment decisions, adherence, and stigma. Establishing a clear relationship between stigma and measurable aspects of treatment adherence and positive health behaviors (e.g., smoking cessation, physical activity, and other beneficial health changes) is needed to guide stigma reduction interventions geared toward enhancement of patient engagement, informed treatment decisions, adherence, and outcomes.

      Survivorship

      In the context of survivorship, multiple cross-sectional studies have established relationships between patient-reported stigma and depression,
      • Gonzalez B.D.
      • Jacobsen P.B.
      Depression in lung cancer patients: the role of perceived stigma.
      lower social functioning,
      • Steffen L.E.
      • Vowles K.E.
      • Smith B.W.
      • Gan G.N.
      • Edelman M.J.
      Daily diary study of hope, stigma, and functioning in lung cancer patients.
      reduced quality of life,
      • Cataldo J.K.
      • Jahan T.M.
      • Pongquan V.L.
      Lung cancer stigma, depression, and quality of life among ever and never smokers.
      and other psychosocial impairment.
      • Chambers S.K.
      • Dunn J.
      • Occhipinti S.
      • et al.
      A systematic review of the impact of stigma and nihilism on lung cancer outcomes.
      • Else-Quest N.M.
      • LoConte N.K.
      • Schiller J.H.
      • Hyde J.S.
      Perceived stigma, self-blame, and adjustment among lung, breast and prostate cancer patients.
      • LoConte N.K.
      • Else-Quest N.M.
      • Eickhoff J.
      • Hyde J.
      • Schiller J.H.
      Assessment of guilt and shame in patients with non–small-cell lung cancer compared with patients with breast and prostate cancer.
      • Shen M.J.
      • Coups E.J.
      • Li Y.
      • Holland J.C.
      • Hamann H.A.
      • Ostroff J.S.
      The role of posttraumatic growth and timing of quitting smoking as moderators of the relationship between stigma and psychological distress among lung cancer survivors who are former smokers.
      • Cataldo J.K.
      • Slaughter R.
      • Jahan T.M.
      • Pongquan V.L.
      • Hwang W.J.
      Measuring stigma in people with lung cancer: psychometric testing of the Cataldo Lung Cancer Stigma Scale.
      Further studies are needed to establish causal connections between stigma, posttreatment surveillance, and other psychosocial/behavioral outcomes, but existing work suggests that stigma has significant intrapersonal effects for patients with lung cancer and lung cancer survivors. Two primary approaches—education and psychotherapy—have shown promise in reducing stigma and psychosocial distress. For example, Brown-Johnson et al.
      • Brown-Johnson C.G.
      • Berrean B.
      • Cataldo J.K.
      Development and usability evaluation of the mHealth Tool for Lung Cancer (mHealth TLC): a virtual world health game for lung cancer patients.
      developed an interactive mobile health tool to address stigma by coaching patients toward assertive communication with health care clinicians. Initial testing with eight patients supported its feasibility and acceptability in practice.
      • Brown-Johnson C.G.
      • Berrean B.
      • Cataldo J.K.
      Development and usability evaluation of the mHealth Tool for Lung Cancer (mHealth TLC): a virtual world health game for lung cancer patients.
      A single-arm, open trial tested an acceptance-focused cognitive behavioral intervention with 14 patients and demonstrated feasibility and initial efficacy with decreases in stigma, cancer distress, and depression.
      • Chambers S.K.
      • Morris B.A.
      • Clutton S.
      • et al.
      Psychological wellness and health-related stigma: a pilot study of an acceptance-focused cognitive behavioural intervention for people with lung cancer.
      It will be important for larger-scale studies to extend these pilot findings and demonstrate utility across multiple psychosocial and behavioral outcomes. Of additional utility will be a review of effective stigma reduction interventions in other health domains (e.g., human immunodeficiency virus [HIV]/acquired immunodeficiency syndrome, substance use, obesity, mental health) to apply a best practices approach to this work. For example, in addition to education and cognitive-behavioral counseling, Cook et al.
      • Cook J.E.
      • Purdie-Vaughns V.
      • Meyer I.H.
      • Busch J.T.A.
      Intervening within and across levels: a multilevel approach to stigma and public health.
      identified the utility of interventions that promote belonging and affirmation of values among stigmatized individuals. Such techniques and strategies may be useful supplements to existing evidence-based psychosocial interventions targeted toward patients with lung cancer.
      • Lehto R.H.
      Psychosocial challenges for patients with advanced lung cancer: interventions to improve well-being.

      An Interpersonal Perspective on Addressing Lung Cancer Stigma

      Consistent with an interpersonal perspective,
      • Cook J.E.
      • Purdie-Vaughns V.
      • Meyer I.H.
      • Busch J.T.A.
      Intervening within and across levels: a multilevel approach to stigma and public health.
      lung cancer stigma is intricately tied to social relationships and perceptions of others. The lung cancer experience involves a complex array of interactions with health care providers, family members, friends, and other caregivers. Stigma has the potential to affect the nature of these social relationships, from content and quality of communication to clinician decision making about treatment, thus emphasizing the importance of addressing social processes in stigma reducing interventions.

      Prevention

      As tobacco use has declined among the general population, smoking has shifted from once being viewed as conventional behavior to now being viewed as an aberrant behavior. In their population survey of New York residents, Stuber et al.
      • Stuber J.
      • Galea S.
      • Link B.G.
      Smoking and the emergence of a stigmatized social status.
      described the negative impact of nonsmoking family and friends’ attitudes on smokers’ perceived stigma. Recent evidence suggests that interpersonal-level stigma from health care providers may also have a negative impact on accurate disclosure of smoking status and other smoking-related discussion.
      • Stuber J.
      • Galea S.
      Who conceals their smoking status from their health care provider?.
      Critical and judgmental assumptions about personal responsibility and blame may diminish the effectiveness of health care providers’ cessation advice, support, and provision of smoking cessation resources.
      • Schroeder S.A.
      What to do with a patient who smokes.
      Browning et al.
      • Browning K.K.
      • Ferketich A.K.
      • Salsberry P.J.
      • Wewers M.E.
      Socioeconomic disparity in provider-delivered assistance to quit smoking.
      reported that only 38% of smokers in their study received assistance with smoking cessation from their medical provider, and strong socioeconomic disparities existed among those offered cessation assistance.
      Given the apparent biases of some primary health care providers,
      • Wassenaar T.R.
      • Eickhoff J.C.
      • Jarzemsky D.R.
      • Smith S.S.
      • Larson M.L.
      • Schiller J.H.
      Differences in primary care clinicians’ approach to non-small cell lung cancer patients compared with breast cancer.
      clinician-focused interventions that promote best practices to provide empathic smoking cessation advice and support are needed. To date, there has also been little work focusing on how friends and family (smokers and nonsmokers) can best support smokers struggling with tobacco dependence, suggesting a clear need for further study and application.

      Screening

      Most studies addressing clinician-level barriers to lung cancer screening (LDCT) referrals have focused on awareness of guidelines, knowledge of survival benefits, and logistical concerns among primary care clinicians.
      • Dunn J.
      • Garvey G.
      • Valery P.C.
      • et al.
      Barriers to lung cancer care: health professionals’ perspectives.
      • Raz D.J.
      • Wu G.X.
      • Consunji M.
      • et al.
      Perceptions and utilization of lung cancer screening among primary care physicians.
      • Hoffman R.M.
      • Sussman A.L.
      • Getrich C.M.
      • et al.
      Attitudes and beliefs of primary care providers in new mexico about lung cancer screening using low-dose computed tomography.
      • Iaccarino J.M.
      • Clark J.
      • Bolton R.
      • et al.
      A national survey of pulmonologists’ views on low-dose computed tomography screening for lung cancer.
      Collectively, this work highlights the connections between limited awareness and lower rates of referrals for lung cancer screening and also emphasizes the need for clinician education about lung cancer screening. However, it is also plausible that underlying stigma and biased attitudes toward screen-eligible patients and clinician nihilism (pessimistic views of individuals at high risk of lung cancer and patients with lung cancer) may bias perceptions of individual patients and limit clinician-initiated discusions and referral patterns for lung cancer screening.
      • Hamann H.A.
      • Lee J.W.
      • Schiller J.H.
      • et al.
      Clinician Perceptions of care difficulty, quality of life, and symptom reports for lung cancer patients: an analysis from the Symptom Outcomes and Practice Patterns (SOAPP) study.
      Given the public health challenges associated with increasing lung cancer screening, it is important to fully elaborate this connection and use the information to tailor clinician-focused education toward engaging appropriate high-risk patients in a discussion about their options for lung cancer screening.
      Relatively little research has evaluated direct interventions to address clinician nihilism, bias, and stigma about initiating discussions regarding lung cancer screening. However, recent efforts to educate clinicians have integrated material to establish social norms regarding the significance and potential importance of lung cancer screening for individual and population health. One continuing education program that was developed and initially tested in Kentucky has demonstrated the preliminary value of direct training for clinicians regarding the benefits and challenges of lung cancer screening.

      Studts JL. Early Efforts to engage clinicians regarding lung cancer screening in Kentucky. Paper presented at: Inaugural Meeting of the National Lung Cancer Roundtable. December 11–12, 2017; Bethesda, MD.

      Mejia MG, Hinchey MC, Byrne MM, Han P, Studts JL. Lung cancer screening: evaluation of a pilot continuing education program for primary care providers. Paper presented at: 35th Annual Meeting and Scientific Sessions of the Society of Behavioral Medicine. April 23–26, 2014; Philadelphia, PA.

      The data showed that clinicians were receptive to the information and benefited from reviewing the data alongside consideration of shared decision making as a platform to explore the option of lung cancer screening. In addition to continuing education efforts, community cancer control specialists from the Kentucky Cancer Program have conducted academic detailing visits as part of the Kentucky Lung Cancer Education, Awareness, Detection, and Survivorship (LEADS) Collaborative with more than 2500 clinicians in an effort to boost lung cancer screening efforts and provide support and tools.

      Kentucky LEADS Collaborative. Kentucky LEADS collaborative: lung cancer education, awareness, detection, survivorship. https://www.kentuckyleads.org/. Accessed February 25, 2018.

      Although these efforts hold promise for indirectly addressing barriers such as nihilism and bias, it may be beneficial to include more overt efforts to discuss and explore concerns related to these important variables. In addition to conducting longer-term evaluations of training programs, it may be important to identify and test training and implementation strategies that more directly address nihilism and bias as barriers both in academic training settings and with practicing clinicians. These interventions can support broader implementation of lung cancer screening and create opportunities to explore the promise of screening in reducing lung cancer nihilism and stigma.

      Diagnosis and Treatment

      To what degree does clinician stigma affect the timing of diagnosis and treatment decisions for patients with lung cancer? In a qualitative study of reasons for delay in diagnosis of lung cancer, general practitioners had differential responses to patients with newly diagnosed lung cancer, reporting sympathy for patients who had never smoked but noting blame toward current smokers.
      • Scott N.
      • Crane M.
      • Lafontaine M.
      • Seale H.
      • Currow D.
      Stigma as a barrier to diagnosis of lung cancer: patient and general practitioner perspectives.
      Innovative work from Wassenaar et al.
      • Wassenaar T.R.
      • Eickhoff J.C.
      • Jarzemsky D.R.
      • Smith S.S.
      • Larson M.L.
      • Schiller J.H.
      Differences in primary care clinicians’ approach to non-small cell lung cancer patients compared with breast cancer.
      demonstrated that general practitioners were less likely to provide evidence-based specialty referrals to patients with lung cancer than to equally staged patients with breast cancer. In this study of primary care clinicians, the researchers compared responses to randomly assigned, identically staged case scenarios of breast and lung cancer. The results indicated that primary care physicians were less likely to refer the patient with advanced-stage lung cancer for further treatment and were also less likely to closely monitor her for uncontrolled pain.
      • Wassenaar T.R.
      • Eickhoff J.C.
      • Jarzemsky D.R.
      • Smith S.S.
      • Larson M.L.
      • Schiller J.H.
      Differences in primary care clinicians’ approach to non-small cell lung cancer patients compared with breast cancer.
      It was suggested that these findings may have been driven by physician nihilism and biased perceptions of lung cancer. In particular, a nihilistic perspective toward the prognosis of patients with lung cancer may result in both the underuse of potentially beneficial therapies and a delay in the widespread adoption of new therapies.
      • Ernani V.
      • Steuer C.E.
      • Jahanzeb M.
      The end of nihilism: systemic therapy of advanced non–small cell lung cancer.
      Although timely access to a cancer specialist after lung biopsy has significant treatment implications,
      • Ganti A.K.
      • Hirsch F.R.
      • Wynes M.W.
      • et al.
      Access to cancer specialist care and treatment in patients with advanced stage lung cancer.
      multiple studies have documented that a significant proportion of patients with advanced lung cancer are not receiving appropriate follow-up care.
      • Ganti A.K.
      • Hirsch F.R.
      • Wynes M.W.
      • et al.
      Access to cancer specialist care and treatment in patients with advanced stage lung cancer.
      • David E.A.
      • Daly M.E.
      • Li C.-S.
      • et al.
      Increasing rates of no treatment in advanced-stage non-small cell lung cancer patients: a propensity-matched analysis.
      One nationwide database study observed that 6% to 10% of patients with newly diagnosed metastatic lung cancer did not receive cancer-directed therapy after positive biopsy results.
      • Ganti A.K.
      • Hirsch F.R.
      • Wynes M.W.
      • et al.
      Access to cancer specialist care and treatment in patients with advanced stage lung cancer.
      Another study used the National Cancer Database and found an increasing rate of patients with advanced-stage NSCLC who are not receiving cancer treatment.
      • David E.A.
      • Daly M.E.
      • Li C.-S.
      • et al.
      Increasing rates of no treatment in advanced-stage non-small cell lung cancer patients: a propensity-matched analysis.
      In addition to its potential impact on decisions about anticancer treatments, stigma may also affect clinician guidance toward ancillary treatment, including advice regarding cessation and referral for evidence-based tobacco treatment. The National Comprehensive Cancer Network has recommended smoking cessation for all smokers who are undergoing treatment for cancer.

      National Comprehensive Cancer Network. NCCN guidelines: smoking cessation. Version 1.2016. https://www.iaslc.org/sites/default/files/wysiwyg-assets/nccn_smoking_0916.pdf. Accessed May 3, 2018.

      Despite the potential “teachable opportunity” associated with diagnosis and treatment, many patients with lung cancer do not receive sufficient support for smoking cessation during these times.
      • Warren G.W.
      • Ward K.D.
      Integration of tobacco cessation services into multidisciplinary lung cancer care: rationale, state of the art, and future directions.
      Although nihilism and pessimistic assumptions about patients' motivation to quit may limit initiation of cessation-based discussions, clinicians may also be hesitant to address smoking cessation because of lack of training and concern about upsetting patients.
      • Stiefel F.
      • Bourquin C.
      Adverse effects of “teachable moment” interventions in lung cancer: why prudence matters.
      Further research is needed to understand how to best manage both the priority of identifying and referring tobacco-dependent patients with lung cancer
      • Dresler C.
      • Warren G.W.
      • Arenberg D.
      • et al.
      “Teachable moment” interventions in lung cancer: why action matters.
      and the importance of maintaining supportive provider-patient relationships. As in clinician-based interventions in the context of screening, addressing clinician roles in timely diagnosis and evidence-based tobacco treatment and referrals will require a focus not only on awareness of the clinical importance of smoking cessation but also on the nature of patient-provider communication to reduce the negative impact of stigma and nihilism.

      Survivorship

      The interpersonal effects of stigma for survivorship, including communication and clinician perceptions, are highly salient and well studied, with important consequences for clinician- and family-focused interventions. In one qualitative study, 48% of patients with lung cancer discussed feeling stigmatized by at least a subset of their medical clinicians.
      • Hamann H.A.
      • Ostroff J.S.
      • Marks E.G.
      • Gerber D.E.
      • Schiller J.H.
      • Lee S.J.C.
      Stigma among patients with lung cancer: a patient-reported measurement model.
      In an investigation of clinician perceptions for more than 3000 patients with solid tumors, researchers found that after adjustment for disease-relevant covariates, clinicians were three times more likely to perceive lower quality of life for their patients with lung cancer.
      • Hamann H.A.
      • Lee J.W.
      • Schiller J.H.
      • et al.
      Clinician Perceptions of care difficulty, quality of life, and symptom reports for lung cancer patients: an analysis from the Symptom Outcomes and Practice Patterns (SOAPP) study.
      These data suggest that perception biases about patients with lung cancer may be related to clinician stigma and nihilism, potentially influencing communication with patients and survivors. Other studies have supported the connection between stigma and interpersonal communication. For example, a large questionnaire study conducted in China revealed that 82% of oncology nurses attributed at least some blame to patients with lung cancer.
      • Wang L.D.-L.
      • Zhan L.
      • Zhang J.
      • Xia Z.
      Nurses’ blame attributions towards different types of cancer: a cross-sectional study.
      In a cross-sectional quantitative study, Shen et al.
      • Shen M.J.
      • Hamann H.A.
      • Thomas A.J.
      • Ostroff J.S.
      Association between patient-provider communication and lung cancer stigma.
      reported that higher levels of patient-reported stigma were associated with poorer patient-clinician communication. Taken together, these studies support the need for stigma reduction interventions to address patient-clinician communication and clinician decision making.
      Physicians and other clinicians who treat patients with lung cancer face numerous communication challenges, including how to communicate effectively in a nonjudgmental and empathic way that empowers patients without exacerbating feelings of self-blame and guilt. In particular, physicians note the challenges of discussing quitting smoking with patients with lung cancer while concurrently managing patients’ emotional distress after diagnosis of cancer and treatment.
      • Warren G.W.
      • Ward K.D.
      Integration of tobacco cessation services into multidisciplinary lung cancer care: rationale, state of the art, and future directions.
      • Stiefel F.
      • Bourquin C.
      Adverse effects of “teachable moment” interventions in lung cancer: why prudence matters.
      • Dresler C.
      • Warren G.W.
      • Arenberg D.
      • et al.
      “Teachable moment” interventions in lung cancer: why action matters.
      Although empathic patient-clinician communication has been associated with lower levels of stigma, health care clinicians may frequently miss opportunities for empathy in lung cancer care.
      • Morse D.S.
      • Edwardsen E.A.
      • Gordon H.S.
      Missed opportunities for interval empathy in lung cancer communication.
      To this end, in a current study on clinician-patient communication in lung cancer care,

      ClinicalTrials.gov. Clinician-patient communication in lung cancer care. http://dx.doi.org/10.1037/sah0000089. Accessed May 2, 2018.

      Ostroff, Banerjee, and their colleagues are testing the impact of empathy-based training for thoracic oncology care physicians and have hypothesized that responding empathically to patients’ discussion of their smoking history may be instrumental to reducing patients’ perceived stigma and may be an effective way to improve disclosure of current smoking status and improve engagement with specialists in tobacco treatment. Current testing focuses on the feasibility and effectiveness of providing training in the skills of empathic communication to oncology care physicians and other health care providers who are treating patients with newly diagnosed lung cancer. The didactic-experiential empathic communication skills module focuses on taking a detailed tobacco history, advising current smokers to quit, and making a reliable referral for tobacco treatment services, all within the context of empathic nonjudgmental interactions with patients. The overall premise is that empathic assessment of smoking status and advising current smokers to quit will reduce perceived and internalized stigma and ultimately improve engagement with evidence-based tobacco treatment and psychosocial support services both during and after treatment of lung cancer.
      The experience of lung cancer can have an overwhelming impact on patients’ relationships with their partners or caregivers, and recent evidence suggests that stigma may play a role in the quality of these relationships. For example, Dirkse et al.
      • Dirkse D.
      • Lamont L.
      • Li Y.
      • Simonič A.
      • Bebb G.
      • Giese-Davis J.
      Shame, guilt, and communication in lung cancer patients and their partners.
      reported that patient-reported shame (a component of internalized stigma) was associated with patients' decreased satisfaction with their relationship with significant others. Similarly, patient-focused blame among lung cancer caregivers is associated with higher depressive symptom scores.
      • Siminoff L.A.
      • Wilson-Genderson M.
      • Baker S.
      Depressive symptoms in lung cancer patients and their family caregivers and the influence of family environment.
      Findings suggest that caregiver-focused interventions in the context of lung cancer should address the impact of stigma and its effects on the caregiving process. A family-centered therapy approach may also be important for families who are struggling with lung cancer blame, guilt, and stigma. In fact, the National Cancer Institute has recently established new research funding opportunities that acknowledge the importance of generating more data to inform clinical practice with regard to supporting cancer caregivers.

      National Cancer Institute. PAR-18–247: Intervening with cancer caregivers to improve patient health outcomes and optimize health care utilization (R21 clinical trial optional). https://grants.nih.gov/grants/guide/pa-files/PAR-18-247.html. Accessed February 25, 2018.

      In the context of lung cancer caregiving, the Kentucky Lung Cancer Education, Awareness, Detection, and Survivorship Collaborative has developed multiple modules that include attention to lung cancer stigma and blame among lung cancer caregivers.

      Studts JL. Development of the Kentucky LEADS Collaborative Lung Cancer Survivorship Care Program. Paper presented at: 38th Annual Meeting and Scientific Sessions of the Society of Behavioral Medicine. March 29–April 1, 2017; San Diego, CA.

      Head B, Andrykowski MA, Burris JL, et al. Development of the Kentucky LEADS Collaborative Lung Cancer Survivorship Care Program. Paper presented at: 17th World Conference of the International Association for the Study of Lung Cancer. December 4–7, 2016; Vienna, Austria.

      The modules, which are designed to address lung cancer-specific stress and social support for survivors and caregivers, include activities that explore efforts to respond to stigmatizing comments and behaviors built on work originally developed by the Lung Cancer Alliance.

      Lung Cancer Alliance. Lung cancer stigma: how to cope. https://lungcanceralliance.org/wp-content/uploads/2017/09/Lung_Cancer_Stigma_How_to_Cope_web.pdf. Accessed March 3, 2018.

      Additionally, the caregiving modules, which are designed to be delivered directly to caregivers in the absence of the lung cancer survivor, involve activities that include attention to stigma as it relates to being an effective caregiver and self-management for caregivers. Outcomes data regarding the impact of these efforts are being collected and will hopefully contribute to the foundation of data that address the challenges presented by stigma and bias for optimal caregiving to individuals with lung cancer and survivor outcomes.

      A Societal Perspective on Addressing Lung Cancer Stigma

      At a societal level, the correlates of stigma relate to understanding and adjusting social conditions, structural components, and public attitudes.
      • Cook J.E.
      • Purdie-Vaughns V.
      • Meyer I.H.
      • Busch J.T.A.
      Intervening within and across levels: a multilevel approach to stigma and public health.
      In the context of lung cancer, stigma can affect the societal level through social attitudes and stereotypes, systems of health care, public health campaigns, funding priorities, and other policy decisions.

      Prevention

      Heralded as one of the leading modern day public health success stories, comprehensive tobacco control efforts, including restrictions on indoor smoking, increased tobacco taxation, and public health national media campaigns

      Centers for Disease Control and Prevention. Best practices for comprehensive tobacco control programs; 2014. https://www.cdc.gov/tobacco/stateandcommunity/best_practices/pdfs/2014/comprehensive.pdf. Accessed February 28, 2018.

      have decreased social acceptance of smoking and collectively contributed to tremendous headway in reducing tobacco use.
      • Cummings K.M.
      • Proctor R.N.
      The changing public image of smoking in the United States: 1964-2014.
      A number of studies have documented substantial societal stigma toward smoking and smokers. Many health initiatives (e.g., smoking bans) have been crucial components of successful population-level tobacco control.

      Centers for Disease Control and Prevention. Best practices for comprehensive tobacco control programs; 2014. https://www.cdc.gov/tobacco/stateandcommunity/best_practices/pdfs/2014/comprehensive.pdf. Accessed February 28, 2018.

      However, some evidence suggests that certain elements of smoking stigma may actually deter individual cessation efforts.
      • Riley K.E.
      • Ulrich M.R.
      • Hamann H.A.
      • Ostroff J.S.
      Decreasing smoking but increasing stigma? Anti-tobacco campaigns, public health, and cancer care.
      For example, social isolation, blaming, and devaluation of smokers may encourage nondisclosure and clandestine smoking and may also limit access to evidence-based tobacco treatment.
      • Chapple A.
      Stigma, shame, and blame experienced by patients with lung cancer: qualitative study.
      In an effort to target tobacco cessation at a societal level, large-scale antitobacco campaigns have focused on hard-hitting messages.

      US Centers for Disease Control and Prevention. Tips from Former Smokers. https://www.cdc.gov/tobacco/campaign/tips/index.html. Accessed March 3, 2018.

      Although these antitobacco campaigns are effective at reducing smoking, they may also unintentionally increase societal stigma toward smokers and patients with lung cancer.
      • Riley K.E.
      • Ulrich M.R.
      • Hamann H.A.
      • Ostroff J.S.
      Decreasing smoking but increasing stigma? Anti-tobacco campaigns, public health, and cancer care.
      There is a growing dialogue as to whether the public health benefits of large-scale antitobacco media campaigns are fully justified in light of the potential for exacerbating stigma toward smokers and patients with lung cancer and other tobacco-related diseases.
      • Davis K.C.
      • Duke J.
      • Shafer P.
      • Patel D.
      • Rodes R.
      • Beistle D.
      Perceived effectiveness of antismoking ads and association with quit attempts among smokers: evidence from the Tips From Former Smokers campaign.
      For instance, although there is strong evidence for the smoking reduction benefits of U.S. Centers for Disease Control and Prevention’s Tips from Former Smokers campaign, which features highly evocative stories of people living with smoking-related diseases, there is also a growing appreciation for the need to better understand the side effects of these interventions and whether these antitobacco campaigns also increase societal stigma toward smokers and, by extension, patients with lung cancer.
      • Riley K.E.
      • Ulrich M.R.
      • Hamann H.A.
      • Ostroff J.S.
      Decreasing smoking but increasing stigma? Anti-tobacco campaigns, public health, and cancer care.
      • Davis K.C.
      • Duke J.
      • Shafer P.
      • Patel D.
      • Rodes R.
      • Beistle D.
      Perceived effectiveness of antismoking ads and association with quit attempts among smokers: evidence from the Tips From Former Smokers campaign.
      Developers of public health media campaigns should consider lung cancer stigma in the development and dissemination of hard-hitting antitobacco media campaigns in a manner akin to how clinician-scientists must monitor for unexpected and undesirable side effects of all our well-intended interventions. Along these lines, the U.S. Food and Drug Administration’s public education campaign Every Try Counts was designed to encourage cigarette smokers to quit by including nonjudgmental messages of support for repeating quitting efforts, with emphasis on the health benefits of quitting and lessons learned from prior quit attempts.

      Screening

      Stigma may be closely intertwined with societal perspectives on lung cancer screening.
      • Carter-Harris L.
      • Gould M.K.
      Multilevel barriers to the successful implementation of lung cancer screening: why does it have to be so hard?.
      Despite the strong and influential data supporting a relative reduction in lung cancer mortality among individuals randomized to the LDCT arm of the National Lung Screening Trial,
      • National Lung Screening Trial Research Team
      • Aberle D.R.
      • Adams A.M.
      • et al.
      Reduced lung-cancer mortality with low-dose computed tomographic screening.
      there has been substantial and vocal public debate as well as considerable opposition to the implementation of lung cancer screening, despite it being a grade B recommendation of the U.S. Preventive Services Task Force.

      US Centers for Medicare & Medicaid Services. Decision memo for screening for lung cancer with low dose computed tomography ( LDCT ) ( CAG-00439N ). 2015:1–90. http://www.cms.gov/medicare-coverage-database/details/nca-decision-memo.aspx?NCAId=274. Accessed May 14, 2018.

      • Woolf S.H.
      • Harris R.P.
      • Campos-Outcalt D.
      Low-dose computed tomography screening for lung cancer.
      On the basis of these lessons from other cancer screening modalities, there is an understandably greater amount of societal attention being paid to the potential harm of lung cancer screening,
      • Harris R.P.
      • Sheridan S.L.
      • Lewis C.L.
      • et al.
      The harms of screening.
      including false-positive results,
      • Pinsky P.F.
      • Bellinger C.R.
      • Miller D.P.
      False-positive screens and lung cancer risk in the National Lung Screening Trial: implications for shared decision-making.
      cost-effectiveness concerns,
      • Puggina A.
      • Broumas A.
      • Ricciardi W.
      • Boccia S.
      Cost-effectiveness of screening for lung cancer with low-dose computed tomography: a systematic literature review.
      and other translational challenges.
      • Gerber D.E.
      • Hamann H.A.
      • Santini N.O.
      • et al.
      Patient navigation for lung cancer screening in an urban safety-net system: protocol for a pragmatic randomized clinical trial.
      In understanding discussions about lung cancer screening, it may also be important to address the subtle and often unintended impact of societal stigma and nihilism that could accompany these considerations and concerns. More research is needed to fully understand whether and how societal stigma and nihilism may be affecting public responses to lung cancer screening, and what can be done to address it.

      Diagnosis and Treatment

      How might societal stigma toward lung cancer affect the structural environment of lung cancer diagnosis and treatment? Although this direct relationship is difficult to connect, it is clear that there are significant disparities in treatment access and treatment research funding for lung cancer.
      • Carter A.J.
      • Nguyen C.N.
      A comparison of cancer burden and research spending reveals discrepancies in the distribution of research funding.
      Progress in the diagnosis and treatment of lung cancer is largely spurred by research funding, but recent discussions have highlighted major disparities for opportunities to address lung cancer in this capacity.

      The ASCO Post. Will funding for lung cancer ever improve? http://www.ascopost.com/issues/september-1-2013/will-funding-for-lung-cancer-ever-improve/. Published 2013. Accessed February 25, 2018.

      In fiscal year 2016, the National Cancer Institute spent $519.9 million for research on breast cancer compared with $283.8 million for research on lung cancer.

      National Cancer Institute. Funding for research areas. https://www.cancer.gov/about-nci/budget/fact-book/data/research-funding. Accessed February 25, 2018.

      This difference in funding likely limits research advances and productivity. A recent worldwide analysis of articles in lung cancer journals concluded that the research base in most countries severely lags behind other cancers.
      • Aggarwal A.
      • Lewison G.
      • Idir S.
      • et al.
      The state of lung cancer research: a global analysis.

      Global Lung Cancer Coalition. Lung cancer research in numbers: briefing for the USA. http://www.lungcancercoalition.org/uploads/docs/Country_briefing_USA_17.06.16[1].pdf. Accessed February 25, 2018.

      On a policy and legislative level, attention to lung cancer diagnosis and treatment is also limited. Although connective empirical data are scarce, patients, clinicians, and advocates have all argued that these policy and funding discrepancies are the result of societal-level stigma and nihilism, creating a self-fulfilling cycle in which lung cancer is viewed as untreatable and patients with lung cancer are not prioritized as deserving to receive the resources needed to advance treatment goals. For example, in an interview-based study of clinicians, most respondents endorsed the belief that societal stigma directly affects funding for lung cancer research.
      • Tran K.
      • Delicaet K.
      • Tang T.
      • Ashley L.B.
      • Morra D.
      • Abrams H.
      Perceptions of lung cancer and potential impacts on funding and patient care: a qualitative study.
      More research using varied methodologies (e.g., vignette-based studies, policy-level analyses) is needed to better understand the connection between research and treatment funding and societal stigma. Addressing these funding and policy discrepancies has been a major focus of lung cancer advocates, who have been promoting legislative action

      Lung Cancer Alliance. Our legislative priorities. https://lungcanceralliance.org/advocacy/our-legislative-priorities/. Accessed February 25, 2018.

      and other policy initiatives that address treatment successes and needs of patients.

      Lung Cancer Alliance. Take action. https://lungcanceralliance.org/advocacy/take-action/. Accessed February 25, 2018.

      Of interest, the emergence of new treatments and communication about their potential benefit may be one way to reduce lung cancer stigma on the societal level.

      Rainone N, Oodal R, Niederdeppe J. The (surprising) impact of televised antidepressant direct-to-consumer advertising on the stigmatization of mental illness. Community Ment Health J. https://doi.org/10.1007/s10597-017-0164-1.

      • Grady D.
      Lung cancer patients live longer with immune therapy.
      Although further research is needed, it may be the case that attention to anticancer agents helps to normalize lung cancer as a treatable illness and reduce the associated stigma. In the emerging landscape of alternative communication platforms, it may also be plausible to leverage social media to change the public perception of lung cancer and the associated stigma.
      • Sutton J.
      • Vos S.C.
      • Olson M.K.
      • et al.
      Lung cancer message on Twitter: content analysis and evaluation.

      Survivorship

      Studies of societal attitudes toward lung cancer survivors underscore the impact that social stigma has on structural forces shaping lung cancer care. A large-scale (N = 1778) general population study of explicit and implicit attitudes (beliefs that may exist outside of conscious awareness) found that participants were more likely to agree with negative descriptive and normative statements about lung cancer than about breast cancer; participants also had significantly stronger implicit negative associations with lung cancer than with breast cancer.
      • Sriram N.
      • Mills J.
      • Lang E.
      • et al.
      Attitudes and stereotypes in lung cancer versus breast cancer.
      Marlow et al.
      • Marlow L.A.V.
      • Waller J.
      • Wardle J.
      Does lung cancer attract greater stigma than other cancer types?.
      randomized a sample of online survey participants to complete a cancer stigma scale related to lung, colorectal, skin, breast, or cervical cancer and found that participants reported the greatest levels of stigma related to lung cancer, with increased perceptions of patients' responsibility for their disease. In another unique study, Luberto et al.
      • Luberto C.M.
      • Hyland K.A.
      • Streck J.M.
      • Temel B.
      • Park E.R.
      Stigmatic and sympathetic attitudes toward cancer patients who smoke: a qualitative analysis of an online discussion board forum.
      used grounded theory to analyze online comments about a study detailing smoking among patients with lung cancer and patients with colorectal cancer. Stigma-based comments were common, with discussions centering on blame and personal responsibility for lung cancer.
      • Luberto C.M.
      • Hyland K.A.
      • Streck J.M.
      • Temel B.
      • Park E.R.
      Stigmatic and sympathetic attitudes toward cancer patients who smoke: a qualitative analysis of an online discussion board forum.
      In terms of public attention and action, Weiss et al.
      • Weiss J.
      • Stephenson B.J.
      • Edwards L.J.
      • Rigney M.
      • Copeland A.
      Public attitudes about lung cancer: stigma, support, and predictors of support.
      conducted a phone survey of 1071 people and asked about the likelihood of their donating money or volunteering time for a cancer organization; 29% of respondents stated that they would likely or very likely donate time and/or money to a breast cancer organization compared with 18% of respondents stating that they would likely or very likely donate time and/or money to a lung cancer organization. Similarly, 25% of respondents selected breast cancer organizations to hypothetically support compared to 12% of respondents who chose lung cancer organizations.
      • Weiss J.
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      • Copeland A.
      Public attitudes about lung cancer: stigma, support, and predictors of support.
      With emerging improvements in lung cancer outcomes, a larger community of lung cancer survivors may emerge and play a larger role in terms of advocacy. As lung cancer survivorship increases and advocacy grows, public support is also expected to increase. However, there is likely to be a continuing need to address societal stigma and its effects on lung cancer survivorship. Advocacy groups have raised awareness of stigma-related concerns in public forums

      American Lung Association. Addressing the stigma of lung cancer. http://www.lung.org/assets/documents/research/addressing-the-stigma-of-lung-cancer.pdf. Accessed May 17, 2018.

      and conferences. Organizations have also launched public awareness campaigns that overtly address the stigma of lung cancer through direct contrasts.

      Adweek. “Deserve to Die” campaign puts lung cancer in spotlight. http://www.adweek.com/creativity/deserve-die-campaign-puts-lung-cancer-spotlight-141508/. Accessed February 25, 2018.

      Future work is needed to establish the impact of such media campaigns on societal attitudes and behaviors. Interventional activity could also heed lessons from efforts to reduce the social stigma of HIV, which focused on promotion of the disease as treatable, along with emphasis on institutional education, community engagement, and presentation of the disease with a human face.
      • Pulerwitz J.
      • Michaelis A.
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      Reducing HIV-related stigma: lessons learned from Horizons research and programs.

      Discussion and Future Directions

      In this analysis, we have comprehensively evaluated the evidence that stigma is an important barrier to achieving the clinical promise of advanced lung cancer care. Our overall findings both extend the analysis of the review by Chambers et al.
      • Chambers S.K.
      • Dunn J.
      • Occhipinti S.
      • et al.
      A systematic review of the impact of stigma and nihilism on lung cancer outcomes.
      and highlight the detrimental role of lung cancer stigma across multiple levels (individual, interpersonal, and societal) and across the entire cancer care continuum (prevention, screening, diagnosis, treatment, and survivorship). Existing research has generally established the connection between lung cancer stigma and outcomes related to treatment and survivorship at both the individual and interpersonal (clinician) levels. It is clear that stigma is associated with increased psychosocial burden for patients with lung cancer and survivors, although the causal mechanisms and potential moderators have not been fully established. Furthermore, the role of stigma and nihilism in clinician communication and perceptions is gaining clarity. Therefore, it is not surprising that both patient-focused
      • Brown-Johnson C.G.
      • Berrean B.
      • Cataldo J.K.
      Development and usability evaluation of the mHealth Tool for Lung Cancer (mHealth TLC): a virtual world health game for lung cancer patients.
      • Chambers S.K.
      • Morris B.A.
      • Clutton S.
      • et al.
      Psychological wellness and health-related stigma: a pilot study of an acceptance-focused cognitive behavioural intervention for people with lung cancer.
      and clinician-focused interventions targeting both individual stigma and relevant communication processes have begun to be developed and tested. Expanded attention to these promising interventions, including a focus on behavioral and clinical care outcomes along with the potential for scalability, is an important future goal (Table 1). Successful sustainability will require further effort to translate evidence-based interventions into clinical care settings and provide useful stigma reduction resources to lung cancer care clinicians.
      Table 1Key interventional needs to address lung cancer stigma across socioecological levels and the cancer care continuum
      Interventional NeedIntrapersonal (Individual/Patient)Interpersonal (Clinician/Family)Societal (Social Attitudes/Policy)
      PreventionTailor smoking cessation interventions for stigmatized smokers

      Acknowledge youth experimentation and nicotine addiction as drivers of persistent smoking
      Address social support techniques for family/friends to adaptively encourage smoking cessation

      Improve strategies for clinician communication and patient engagement in tobacco treatment
      Consider lung cancer stigma in the development of messaging for antitobacco media campaigns
      ScreeningAddress stigma in developing patient decision aids for lung cancer screening

      Consider messaging in screening decision aids and tailor by smoking status in efforts to decrease stigma
      Expand clinician-level information about lung cancer screening

      Overtly discuss stigma and nihilism with clinicians in training and practice
      Consider addressing stigma in development of public campaigns and materials focused on lung cancer screening

      Work with advocacy groups to change the public conversation about stigma related to those at risk for lung cancer
      Diagnosis/treatmentDevelop patient-focused stigma reduction modules/interventions to facilitate timely diagnosis, treatment adherence, and other positive health behaviors (e.g., smoking cessation)Directly address clinician nihilism in education that promotes evidence-based referral and treatment informationPromote societal understanding of lung cancer by highlighting diagnosis and treatment options, including the benefits of tobacco cessation on cancer treatment outcomes
      SurvivorshipContinue establishing the effectiveness of patient-focused education and counseling on reducing stigma, psychosocial distress, and adherence to survivorship guidelinesContinue training focused on clinician empathy and communication with patients with lung cancer

      Expand efforts to support caregivers of patients with lung cancer
      Expand advocacy efforts that highlight experiences of lung cancer survivors and promote policy change
      Understanding the multilevel role of stigma in the context of prevention, screening, and early detection is a crucial area for future study to realize the full benefits offered by cancer prevention and control in these areas. Existing research has documented stigma as a barrier to patient-clinician discussions about smoking, the decision to screen (or not screen) for lung cancer, and actual screening behavior. There is a distinct and exceptional opportunity at this relatively early stage of implementation of lung cancer screening to design interventions that both leverage the ability to identify stigma and intervene in this vulnerable patient population (see Table 1). Across all phases of the cancer control continuum, it will be important to further understand the impact of societal-level stigma (related to both smoking and lung cancer) on discrepancies in policy, legislation, and funding. Partnerships between patient advocates and lung cancer researchers can help elucidate and address these issues through discussions about evidence-based messaging and measurement of message impact, along with greater exposure to legislative strategies (see Table 1). Progress has already been made, with changes to antismoking media campaigns that emphasize empathy and positive behavioral support along with introduction of lung cancer–focused legislative efforts. As cancer control moves forward in lung cancer specifically, it is imperative to realize that stigma is a multilevel phenomenon that can be addressed only by multilevel approaches involving elements of a socioecological framework as guides to study and implementation.
      Coordinated, interdisciplinary, and well-conceptualized efforts have the potential to reduce the barrier of stigma in the context of lung cancer and facilitate demonstrable improvements in clinical care and quality of life. The understanding of stigma as it relates to lung cancer is relatively recent, but the focus on stigma in other disease domains, including HIV/acquired immunodeficiency syndrome, has a robust literature and history. Although it will be important to understand issues and needs specific to lung cancer, attention to successful stigma reduction interventions and lessons learned in other domains will also be an important element to consider and integrate. There is a unique opportunity to be proactive rather than reactive in this arena. Successfully addressing stigma is an important step in fulfilling the promise to reduce the burden of lung cancer.

      Acknowledgments

      Research reported in this publication was supported by the NCI Cancer Center Support Grant developmental funds of the University of Arizona under award number P30CA023074. Additional support was provided by the Bristol-Myers Squibb Foundation (to Dr. Studts), and the Kentucky Lung Cancer Research Program (to Dr. Studts). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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