Advertisement

Patients’ Knowledge, Beliefs, and Distress Associated with Detection and Evaluation of Incidental Pulmonary Nodules for Cancer: Results from a Multicenter Survey

Open ArchivePublished:March 06, 2016DOI:https://doi.org/10.1016/j.jtho.2016.01.018

      Abstract

      Introduction

      Pulmonary nodules are detected in more than 1 million Americans each year. Prior qualitative work suggests that the detection of incidental pulmonary nodules can be burdensome for patients, but whether these findings generalize to a broader sample of patients is unknown. We categorized patients’ knowledge, beliefs, and distress associated with detection and evaluation of a pulmonary nodule, as well as their impressions of clinician communication.

      Methods

      We administered a cross-sectional survey to adults with an incidental pulmonary nodule who were recruited from a rural medical center, an urban safety net hospital, and a Veterans Affairs hospital.

      Results

      Of the 490 individuals mailed surveys, 244 (50%) responded. Median nodule size was 7 mm, mean patient age was 67 years, 29% of respondents were female, and 86% were white. A quarter of the respondents (26%) reported clinically significant distress related to their nodule, our primary outcome, as measured by the Impact of Event Scale. Patients reported multiple concerns, including uncertainty about the nodule’s cause (78%), the possibility of cancer (73%), and the possible need for surgery (64%). Only 25% of patients accurately estimated their lung cancer risk (within 15% of their actual risk); overall, there was no correlation between perceived and actual risk (r = –0.007, p = 0.93). The 23% of patients who did receive information on cancer risk from their provider were more likely to find this information reassuring (16%) than scary (7%).

      Conclusion

      A quarter of patients with incidental pulmonary nodules experienced clinically significant distress. Knowledge about cancer risk and evaluation was poor. Clinician communication may help bridge knowledge gaps and alleviate distress in some patients.

      Keywords

      Introduction

      More than 1.5 million Americans are found to have a new pulmonary nodule each year through incidental detection, and these numbers are expected to rise further with adoption of lung cancer screening.
      • Aberle D.R.
      • Adams A.M.
      • et al.
      National Lung Screening Trial Research Team
      Reduced lung-cancer mortality with low-dose computed tomographic screening.
      • Gould M.K.
      • Tang T.
      • Liu I.A.
      • et al.
      Recent trends in the identification of incidental pulmonary nodules.
      When a nodule is detected, clinicians must convey to the patient what the nodule is (i.e., the possibility of cancer, which is less than 5% for most patients) and how the nodule will be evaluated.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      What do you mean, a spot?: a qualitative analysis of patients' reactions to discussions with their physicians about pulmonary nodules.
      For most patients, evaluation will entail a 2-year course of radiographic surveillance to ensure that the nodule is not enlarging; guidelines suggest reserving invasive procedures for those with a higher risk for cancer.
      • Gould M.K.
      • Fletcher J.
      • Iannettoni M.D.
      • et al.
      Evaluation of patients with pulmonary nodules: when is it lung cancer?: ACCP evidence-based clinical practice guidelines (2nd edition).
      • MacMahon H.
      • Austin J.H.
      • Gamsu G.
      • et al.
      Guidelines for management of small pulmonary nodules detected on CT scans: a statement from the Fleischner Society.
      • Callister M.E.
      • Baldwin D.R.
      • Akram A.R.
      • et al.
      British thoracic society guidelines for the investigation and management of pulmonary nodules.
      Given how often pulmonary nodules are found, it is important that clinicians understand the experience and concerns of patients with pulmonary nodules and be prepared to discuss them.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      What do you mean, a spot?: a qualitative analysis of patients' reactions to discussions with their physicians about pulmonary nodules.
      • Slatore C.G.
      • Au D.H.
      • Press N.
      • Wiener R.S.
      • Golden S.E.
      • Ganzini L.
      Decision making among veterans with incidental pulmonary nodules: a qualitative analysis.
      • Slatore C.G.
      • Press N.
      • Au D.H.
      • Curtis J.R.
      • Wiener R.S.
      • Ganzini L.
      What the heck is a “nodule”? A qualitative study of veterans with pulmonary nodules.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      ‘The thing is not knowing': Patients' perspectives on surveillance of an indeterminate pulmonary nodule.
      Yet, how the experience of nodule detection and evaluation affects patients is not entirely clear. Qualitative studies and a single-center survey of patients with incidentally detected nodules suggest that detection and evaluation can lead to distress and reduced quality of life in some cases.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      What do you mean, a spot?: a qualitative analysis of patients' reactions to discussions with their physicians about pulmonary nodules.
      • Slatore C.G.
      • Press N.
      • Au D.H.
      • Curtis J.R.
      • Wiener R.S.
      • Ganzini L.
      What the heck is a “nodule”? A qualitative study of veterans with pulmonary nodules.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      ‘The thing is not knowing': Patients' perspectives on surveillance of an indeterminate pulmonary nodule.
      • Slatore C.G.
      • Golden S.E.
      • Ganzini L.
      • Wiener R.S.
      • Au D.H.
      Distress and patient-centered communication among veterans with incidental (not screen-detected) pulmonary nodules. A cohort study.
      However, whether these results are generalizable is unknown. Recognizing the increasing emphasis on patient-centered care and the growing numbers of patients with pulmonary nodules, the American Thoracic Society recently called for more research to explore the impact of nodule detection on patients.
      • Slatore C.G.
      • Horeweg N.
      • Jett J.R.
      • et al.
      An official American Thoracic Society research statement: a research framework for pulmonary nodule evaluation and management.
      We sought to more fully characterize the psychosocial impact of nodule detection and evaluation with a survey of patients with incidental pulmonary nodules managed at three diverse clinical sites in the northeastern United States. We hypothesized that a subset of patients would report substantial nodule-related distress and that misperceptions regarding pulmonary nodules and their evaluation would be common.

      Materials and Methods

      All study procedures were approved by the institutional review boards at the three sites.

      Study Population

      Participants were recruited from three diverse sites: Boston Medical Center, an inner-city safety net medical center; Dartmouth-Hitchcock Medical Center (DHMC), a tertiary care center in a rural setting; and the Veterans Affairs (VA) Boston Healthcare System, a large urban VA hospital. Eligible participants were English-speaking adults (between the ages of 8 and 89 years) who had been found to have a pulmonary nodule smaller than 3 cm within the 3 years before survey administration. Eligible participants were identified through three methods: (1) computerized search of chest imaging reports for terms such as pulmonary nodule; (2) computerized search of clinicians’ problem lists for the term pulmonary nodule; and (3) manual review of a clinical registry of patients with pulmonary nodules.

      Survey Instrument

      We designed a self-administered questionnaire to cover topics in six domains: (1) nodule-specific knowledge, (2) nodule-specific distress, (3) health behavior, (4) nodule management preferences, (5) patient-clinician communication, and (6) patient characteristics. Within these domains we identified the issues of greatest relevance to patients through a series of four focus groups at two sites (Boston Medical Center and DHMC) and developed survey items to probe these issues.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      What do you mean, a spot?: a qualitative analysis of patients' reactions to discussions with their physicians about pulmonary nodules.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      ‘The thing is not knowing': Patients' perspectives on surveillance of an indeterminate pulmonary nodule.
      The draft survey instrument was tested for content, clarity, and comprehensibility through a series of pilot tests. First, we sought feedback from three experts on survey research and 13 content experts from two medical centers (eight pulmonologists and five primary care providers). Next, we administered the survey to a convenience sample of 13 patients with incidentally detected pulmonary nodules who had been seen in the DHMC pulmonary clinic. Finally, we performed in-depth cognitive interviews with three patients with pulmonary nodules. The survey was iteratively revised in response to feedback from each of these steps. The final survey instrument consisted of 46 items and included both validated scales and novel questions (see Survey, Supplementary Digital Content 1, for the complete survey questions).
      • Little P.
      • Everitt H.
      • Williamson I.
      • et al.
      Observational study of effect of patient centredness and positive approach on outcomes of general practice consultations.
      • Horowitz M.
      • Wilner N.
      • Alvarez W.
      Impact of event scale: a measure of subjective stress.

      Survey Administration

      We mailed the survey to eligible participants between July 2011 and December 2012. Mailed reminders regarding survey completion were sent after weeks 2 and 4. Participants who returned surveys received a small incentive (a $10–$15 gift card).

      Outcome Measures

      Our primary outcome was nodule-specific distress, as determined on the basis of Impact of Event Scale, a validated 15-item measure of distress related to a specific event (i.e., nodule detection) that is composed of two subscales: intrusion (intrusive thoughts) and avoidance (actively staying away from reminders of the nodule).
      • Horowitz M.
      • Wilner N.
      • Alvarez W.
      Impact of event scale: a measure of subjective stress.
      • Joseph S.
      Psychometric evaluation of Horowitz's Impact of Event Scale: a review.
      We selected this measure to allow direct comparisons with other studies of patients with incidentally detected and screen-detected nodules.
      • Slatore C.G.
      • Golden S.E.
      • Ganzini L.
      • Wiener R.S.
      • Au D.H.
      Distress and patient-centered communication among veterans with incidental (not screen-detected) pulmonary nodules. A cohort study.
      • van den Bergh K.A.
      • Essink-Bot M.L.
      • Borsboom G.J.
      • Scholten E.T.
      • van Klaveren R.J.
      • de Koning H.J.
      Long-term effects of lung cancer computed tomography screening on health-related quality of life: The NELSON trial.
      • Taylor K.L.
      • Shelby R.
      • Gelmann E.
      • McGuire C.
      Quality of life and trial adherence among participants in the prostate, lung, colorectal, and ovarian cancer screening trial.
      Scores range from 0 to 75, with higher scores indicating more distress. As in prior studies of cancer-related distress,
      • Landsbergen K.M.
      • Prins J.B.
      • Brunner H.G.
      • Hoogerbrugge N.
      Shortened time interval between colorectal cancer diagnosis and risk testing for hereditary colorectal cancer is not related to higher psychological distress.
      • Fiscella K.
      • Whitley E.
      • Hendren S.
      • et al.
      Patient navigation for breast and colorectal cancer treatment: a randomized trial.
      • Shoma A.M.
      • Mohamed M.H.
      • Nouman N.
      • et al.
      Body image disturbance and surgical decision making in Egyptian post menopausal breast cancer patients.
      • Butow P.N.
      • Fardell J.E.
      • Smith A.
      Fear of cancer recurrence: an overview and Australian perspective.
      we used the recommended categories of normal (score 0–8) or mild (9–25), moderate (26–43), or severe (44–75) distress, with clinically significant distress defined as moderate or severe (score ≥26).
      We measured perceived lung cancer risk using a simple visual analogue scale that ranged from 0 in 100 (labeled as “0%, no chance”) to 100 in 100 (“100% certainty”) and was marked in 10% increments. Respondents were instructed to “place an X on the part of the scale that matches your best guess about how likely it is that the spot in your lung will turn out to be cancer.” Misperception of lung cancer risk was defined as an absolute discrepancy of 15% or greater between patients' self-estimated risk for a malignant nodule and their actual risk calculated using the Mayo model, a validated model that estimates risk for a pulmonary nodule being cancerous on the basis of both radiographic and patient characteristics.
      • Swensen S.J.
      • Silverstein M.D.
      • Ilstrup D.M.
      • Schleck C.D.
      • Edell E.S.
      The probability of malignancy in solitary pulmonary nodules. Application to small radiologically indeterminate nodules.
      We assessed the perceived quality of communication with clinicians using the Communication and Partnership subscale of Little’s Measure of Patient-Centered Communication,
      • Little P.
      • Everitt H.
      • Williamson I.
      • et al.
      Observational study of effect of patient centredness and positive approach on outcomes of general practice consultations.
      an instrument recommended in a prior systematic review.
      • Hudon C.
      • Fortin M.
      • Haggerty J.L.
      • Lambert M.
      • Poitras M.E.
      Measuring patients' perceptions of patient-centered care: a systematic review of tools for family medicine.
      We also asked about specific clinician communication strategies and psychosocial factors that may moderate the distress evoked by a nodule.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      What do you mean, a spot?: a qualitative analysis of patients' reactions to discussions with their physicians about pulmonary nodules.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      ‘The thing is not knowing': Patients' perspectives on surveillance of an indeterminate pulmonary nodule.

      Statistical Analyses

      All analyses were performed using Stata software (StataCorp LP, College Station, TX). Multiple descriptive statistics were obtained from the survey data: categorical, ordinal, and dichotomous variables were reported as proportions and relative frequencies, whereas continuous variables were reported as means plus or minus SD or medians with interquartile ranges (IQRs). Participants with missing data for individual survey items were excluded from analyses including those variables. Participants with known lung cancer were excluded from analyses assessing knowledge about likelihood of cancer and natural history of pulmonary nodules, knowledge about pulmonary nodule evaluation, and impact on emotional health and behavior.
      We compared each subject’s actual lung cancer risk estimated by the Mayo model with the patient’s perceived cancer risk using Spearman's correlation coefficient. Multivariable logistic regression models were used to determine factors associated with clinically significant nodule-related distress, excluding patients with lung cancer or missing data for this variable. We first used bivariate analyses to assess associations of patient variables (e.g., age, sex, education, financial pressures, smoking status, comorbidities, time since nodule detection, and misperception of cancer risk) with clinically significant nodule-related distress. Those factors moderately associated with distress in bivariate analyses (p < 0.1) were included in the multivariable model.

      Results

      Of 490 eligible patients who were mailed the survey, 244 patients (49.7%) participated. Their mean age was 66.7 (SD 11.6), 29% were female, and 86% were white. The median nodule size was 7 mm (IQR 5–10). Eighteen patients (7%) reported a diagnosis of lung cancer. Reflecting the low socioeconomic status of our sample, respondents had a high degree of financial insecurity (58%) and disproportionately high rates of tobacco use (78% were current or former smokers [Table 1]).
      Table 1Characteristics of Survey Respondents (n = 244)
      CharacteristicValue
      Mean age ± SD, y67 ± 12
      Median nodule size (IQR), mm7 (5–10)
      Time since nodule detection
       ≤1 y30%
       1–2 y38%
       >2 years32%
      Female,29%
      Race/ethnicity
       White86%
       Black10%
       Hispanic1%
       Native American2%
      Highest level of education
       Some high school18%
       High school diploma32%
       Some college29%
       College diploma or higher21%
      Enough money to pay bills58%
      Married or significant other53%
      Children in home9%
      Smoking status
       Current30%
       Former48%
      Anxiety or depression44%
      Personal diagnosis of
       Chronic obstructive pulmonary disease43%
       Lung cancer7%
       Non-lung cancer13%
      Friends or family with lung cancer31%
      SD, standard deviation; IQR, interquartile range.

      Knowledge about the Likelihood of Cancer and the Natural History of Pulmonary Nodules

      Misperceptions of lung cancer risk were common. Only a quarter (25%) of respondents estimated their cancer risk accurately (within 15 percentage points); most grossly overestimated the likelihood of a malignant nodule. Whereas the median perceived risk for lung cancer was 20% (IQR 10–50%), the median actual risk estimated by the Mayo model
      • Swensen S.J.
      • Silverstein M.D.
      • Ilstrup D.M.
      • Schleck C.D.
      • Edell E.S.
      The probability of malignancy in solitary pulmonary nodules. Application to small radiologically indeterminate nodules.
      was 7.1% (IQR 4.6–10.3%). There was no correlation between patients’ perceived risk for lung cancer and their actual risk (Spearman’s rho = –0.007, p = 0.93 [Fig. 1A]).
      Figure thumbnail gr1
      Figure 1Correlation of patient’s perceived risk for lung cancer to both actual risk (A) and distress (B). The x axis in (A) and (B) represents patients' perceived risk for lung cancer. Perceived risk was moderately correlated with distress (Spearman's rho = 0.33, p < 0.001) but not to actual risk (Spearman’s rho = −0.007, p = 0.93). IQR, interquartile range.
      Patients also had misperceptions about the natural history of pulmonary nodules. A substantial minority (41%) believed that, if untreated, the nodule would turn into cancer. Three-quarters of patients (71%) were unaware of the possibility of indolent tumors (“lung cancers that grow so slowly they are unlikely to cause problems in your lifetime”). Although most small nodules are asymptomatic, half of the patients (50%) believed that their nodule caused shortness of breath. Similarly, patients commonly attributed cough (41%) or pain (back pain in 27% of cases and chest pain in 24%) to the nodule.

      Knowledge about Nodule Evaluation

      Although the typical duration of surveillance recommended to rule out malignancy is 2 to 3 years,
      • Gould M.K.
      • Fletcher J.
      • Iannettoni M.D.
      • et al.
      Evaluation of patients with pulmonary nodules: when is it lung cancer?: ACCP evidence-based clinical practice guidelines (2nd edition).
      • MacMahon H.
      • Austin J.H.
      • Gamsu G.
      • et al.
      Guidelines for management of small pulmonary nodules detected on CT scans: a statement from the Fleischner Society.
      many patients believed they needed longer follow-up: 7% of patients believed that the nodule would be followed up for about 5 years and 32% for the rest of their lives. Many would feel uncomfortable stopping surveillance (10% would feel “extremely nervous” and 29% “somewhat nervous”) even if their doctor told them that no further computed tomography (CT) scans were needed.

      Impact on Emotional Health and Behavior

      Nodule-related distress was common. Half of patients reported distress: 27% mild and 24% clinically significant distress (12% moderate and 12% severe). Distress was moderately correlated with perceived risk for lung cancer (Spearman's rho = 0.33, p < 0.0010 [Fig. 1B]) but was only weakly correlated with actual lung cancer risk (Spearman's rho = –0.19, p = 0.01 [data not shown]). Although multiple patient characteristics were associated with clinically significant distress in bivariate analyses (Table 2), only financial insecurity (“not having enough money to pay the bills”; adjusted OR = 4.0, 95% confidence interval [CI]: 1.2–13.5) and current tobacco use (adjusted OR = 3.5, 95% CI: = 1.2–9.6) were significantly associated with clinically significant distress in multivariable regression analysis. Time since nodule detection was not significantly associated with distress in bivariate analysis and was therefore not included in the multivariable model.
      Table 2Factors Associated with Clinically Significant Distress among Patients with an Indeterminate Pulmonary Nodule
      Patient CharacteristicBivariate AnalysesMultivariable Regression
      OR (95% CI), p ValueOR (95% CI), p Value
      Age >65 y0.5 (0.2–1.0), 0.060.7 (0.2–1.9), 0.44
      Has a significant other0.5 (0.2–1.1), 0.070.6 (0.2–1.7), 0.31
      History of anxiety or depression3.3 (1.5–7.3), 0.0032.3 (0.7–7.3), 0.16
      Not enough money to pay bills8.6 (3.5–21.4), <0.0014.0 (1.2–13.5), 0.03
      Current smoker3.8 (1.7–8.5), 0.0013.5 (1.2–9.6), 0.02
      High school diploma or less2.1 (1.0–4.5), 0.061.1 (0.4–3.1), 0.92
      White race0.2 (0.1–0.5), 0.0010.5 (0.1–2.0), 0.33
      Perceived risk cancer (by quartile)
      Quartile 1, <10%; quartile 2, 10%–19%; quartile 3: 20%–49%; quartile 4: ≥50%.
      1.8 (1.2–2.5), 0.0031.4 (0.8–2.2), 0.2
      Note: Excluding patients whose nodule had been determined to be malignant.
      OR, odds ratio; CI, confidence interval.
      a Quartile 1, <10%; quartile 2, 10%–19%; quartile 3: 20%–49%; quartile 4: ≥50%.
      In addition, a substantial proportion of patients expressed other negative emotions related to their nodule: 62% of patients reported fear while waiting for CT scan results (8% described the wait as “some of the scariest times in my life,” 11% as “very scary,” 15% as “somewhat scary,” and 28% as “a little scary”), and 37% worried about the nodule (12% “often” and 25% “sometimes”). A quarter of patients felt overwhelmed when thinking about the nodule (9% often and 14% sometimes).
      Patients reported a variety of concerns about the nodule. The majority expressed concern about not knowing what the nodule was (78%), lack of control over what happens (66%), and the possibility of cancer (73%), but concerns about evaluation were also common (Fig. 2). Some reported changes in their emotional well-being or in the activities they engaged in after the nodule was discovered (Fig. 3). Although some changes were negative (e.g., 24% reported feeling more anxious and 18% more sad), others were healthy (e.g., 35% reported quitting smoking). Despite the tolls of nodule detection, the vast majority of respondents (93%) were glad they found out about the nodule.
      Figure thumbnail gr2
      Figure 2Patients' concerns related to a pulmonary nodule. CAT, computerized axial tomography.
      Figure thumbnail gr3
      Figure 3Psychosocial changes attributed to a pulmonary nodule.

      Preferences for Decision Making and Perceptions of Communication with Clinicians

      Most respondents (80%) indicated a preference for shared decision making with their physician. In general, respondents rated their doctors’ patient-centered communication skills highly (mean score 3.9, SD 0.8; range of possible scores 1-5, with higher scores indicating more patient-centered communication).
      • Little P.
      • Everitt H.
      • Williamson I.
      • et al.
      Observational study of effect of patient centredness and positive approach on outcomes of general practice consultations.
      However, when asked about nodule-specific communication interventions that prior work has suggested may be helpful,
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      What do you mean, a spot?: a qualitative analysis of patients' reactions to discussions with their physicians about pulmonary nodules.
      • Slatore C.G.
      • Golden S.E.
      • Ganzini L.
      • Wiener R.S.
      • Au D.H.
      Distress and patient-centered communication among veterans with incidental (not screen-detected) pulmonary nodules. A cohort study.
      patients reported variable performance (Fig. 4). Although most (70%) reported that their doctor told them the nodule’s size, many indicated that their clinicians did not show them their CT (48%), provide specific cancer risk information (61%), or reassure them that nodules are common (39%). For the patients who did receive these nodule-specific communication strategies, most found them reassuring rather than anxiety provoking (Fig. 4).
      Figure thumbnail gr4
      Figure 4Nodule-specific communication strategies. CT, computed tomography.

      Discussion

      To our knowledge this is the first multicenter study exploring the patient experience with incidental pulmonary nodules in the United States. We found that misconceptions about nodules and their evaluation were common, and that a quarter of patients experienced clinically significant nodule-related distress. For some patients the distress was severe enough to alter their behavior as though they had limited time to live (e.g., cutting back at work, spending more time with loved ones [Fig. 3]). Patients' perceptions of cancer risk were more strongly correlated with distress than was actual cancer risk, highlighting the need to improve communication to rectify patient overestimates of the likelihood of cancer. Indeed, certain nodule-specific communication strategies appeared to be reassuring to some patients.
      These data corroborate and help quantify the impact of incidental nodule detection on emotional health and quality of life that was observed in prior studies.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      What do you mean, a spot?: a qualitative analysis of patients' reactions to discussions with their physicians about pulmonary nodules.
      • Slatore C.G.
      • Au D.H.
      • Press N.
      • Wiener R.S.
      • Golden S.E.
      • Ganzini L.
      Decision making among veterans with incidental pulmonary nodules: a qualitative analysis.
      • Slatore C.G.
      • Press N.
      • Au D.H.
      • Curtis J.R.
      • Wiener R.S.
      • Ganzini L.
      What the heck is a “nodule”? A qualitative study of veterans with pulmonary nodules.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      ‘The thing is not knowing': Patients' perspectives on surveillance of an indeterminate pulmonary nodule.
      • Slatore C.G.
      • Golden S.E.
      • Ganzini L.
      • Wiener R.S.
      • Au D.H.
      Distress and patient-centered communication among veterans with incidental (not screen-detected) pulmonary nodules. A cohort study.
      • Sullivan D.R.
      • Golden S.E.
      • Ganzini L.
      • Hansen L.
      • Slatore C.G.
      ‘I still don't know diddly': a longitudinal qualitative study of patients' knowledge and distress while undergoing evaluation of incidental pulmonary nodules.
      • Lemonnier I.
      • Baumann C.
      • Jolly D.
      • et al.
      Solitary pulmonary nodules: consequences for patient quality of life.
      Yet, our results differ somewhat from those in the literature on the impact of screen-detected pulmonary nodules.
      • van den Bergh K.A.
      • Essink-Bot M.L.
      • Borsboom G.J.
      • Scholten E.T.
      • van Klaveren R.J.
      • de Koning H.J.
      Long-term effects of lung cancer computed tomography screening on health-related quality of life: The NELSON trial.
      • Gareen I.F.
      • Duan F.
      • Greco E.M.
      • et al.
      Impact of lung cancer screening results on participant health-related quality of life and state anxiety in the National Lung Screening Trial.
      • Kaerlev L.
      • Iachina M.
      • Pedersen J.H.
      • Green A.
      • Norgard B.M.
      CT-screening for lung cancer does not increase the use of anxiolytic or antidepressant medication.
      • Slatore C.G.
      • Sullivan D.R.
      • Pappas M.
      • Humphrey L.L.
      Patient-centered outcomes among lung cancer screening recipients with computed tomography: a systematic review.
      Some lung cancer screening trials do suggest that patients experience mild short-term distress,
      • van den Bergh K.A.
      • Essink-Bot M.L.
      • Borsboom G.J.
      • Scholten E.T.
      • van Klaveren R.J.
      • de Koning H.J.
      Long-term effects of lung cancer computed tomography screening on health-related quality of life: The NELSON trial.
      anxiety,
      • Byrne M.M.
      • Weissfeld J.
      • Roberts M.S.
      Anxiety, fear of cancer, and perceived risk of cancer following lung cancer screening.
      or impairments in quality of life
      • Mazzone P.J.
      • Obuchowski N.
      • Fu A.Z.
      • Phillips M.
      • Meziane M.
      Quality of life and healthcare use in a randomized controlled lung cancer screening study.
      after nodule detection. But in the National Lung Screening Trial (the largest study of lung cancer screening), there was no significant change in anxiety or quality of life among patients with a screen-detected nodule compared with those with normal screening tests results.
      • Gareen I.F.
      • Duan F.
      • Greco E.M.
      • et al.
      Impact of lung cancer screening results on participant health-related quality of life and state anxiety in the National Lung Screening Trial.
      What explains the differences between the transient disturbances in nodule-related distress and anxiety among patients with pulmonary nodules observed in some lung cancer screening trials and the larger impact observed among those with incidentally detected nodules in this and other studies? One possibility is that the perceptions (or expectations) of patients undergoing lung cancer screening are different from those of patients with incidental nodules who are cared for in usual practice. Subjects in clinical trials tend to receive more thorough communication than is typical in usual practice; in particular, subjects in lung cancer screening studies were likely to have been counseled regarding the possibility of nodule detection before the screening CT scan. By contrast, patients with an incidentally detected nodule would not typically be counseled in advance that a nodule might be found, as the CT is by definition performed for another reason. Another possibility is that subjects in clinical trials may be different from the patients we surveyed. We specifically sought to survey patients from populations that are typically underrepresented in clinical trials, allowing us to explore the influence of psychosocial stressors.
      Indeed, we found financial instability and current tobacco use, both of which disproportionately plague patients with low socioeconomic status, to be associated with clinically significant nodule-related distress. Financial hardship is increasingly recognized as a determinant of health status and morbidity in a variety of disease states.
      • Adler N.E.
      • Stead W.W.
      Patients in context—EHR capture of social and behavioral determinants of health.
      • Franks P.
      • Tancredi D.J.
      • Winters P.
      • Fiscella K.
      Including socioeconomic status in coronary heart disease risk estimation.
      Committee on the Recommended Social and Behavioral Domains and Measures for Electronic Health Records, Board on Population Health and Public Health Practice, Institute of Medicine
      Capturing Social and Behavioral Domains and Measures in Electronic Health Records: Phase 2.
      • Walker R.J.
      • Smalls B.L.
      • Campbell J.A.
      • Strom Williams J.L.
      • Egede L.E.
      Impact of social determinants of health on outcomes for type 2 diabetes: a systematic review.
      In the context of nodule detection, patients may be distressed by the fear of the financial strain and loss of income associated with a potential diagnosis of lung cancer. The financial burden associated with testing and treatment of pulmonary nodules and screen-detected cancers has been identified as a potential patient-centered harm of lung cancer screening.
      • Harris R.P.
      • Sheridan S.L.
      • Lewis C.L.
      • et al.
      The harms of screening: a proposed taxonomy and application to lung cancer screening.
      • Jonnalagadda S.
      • Bergamo C.
      • Lin J.J.
      • et al.
      Beliefs and attitudes about lung cancer screening among smokers.
      Prior surveys have shown conflicting effects of current smoking on nodule-related distress: although one small study suggested no effect,
      • Slatore C.G.
      • Golden S.E.
      • Ganzini L.
      • Wiener R.S.
      • Au D.H.
      Distress and patient-centered communication among veterans with incidental (not screen-detected) pulmonary nodules. A cohort study.
      others are consistent with our finding of higher levels of distress and anxiety among current smokers after nodule detection.
      • van den Bergh K.A.
      • Essink-Bot M.L.
      • Borsboom G.J.
      • Scholten E.T.
      • van Klaveren R.J.
      • de Koning H.J.
      Long-term effects of lung cancer computed tomography screening on health-related quality of life: The NELSON trial.
      • Byrne M.M.
      • Weissfeld J.
      • Roberts M.S.
      Anxiety, fear of cancer, and perceived risk of cancer following lung cancer screening.
      Some of the distress our patients experienced may be related to commonly held misconceptions about pulmonary nodules and their evaluation. Patients had a poor understanding of the natural history of nodules, associated symptoms, and duration of surveillance. Although patients cited many causes of distress, most patients cited uncertainty in diagnosis, lack of control, and fear of cancer as serious concerns. This survey again highlights the psychological toll that uncertainty can cause
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      ‘The thing is not knowing': Patients' perspectives on surveillance of an indeterminate pulmonary nodule.
      and the importance of supporting patients through the potentially distressing period of nodule surveillance.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      What do you mean, a spot?: a qualitative analysis of patients' reactions to discussions with their physicians about pulmonary nodules.
      • Slatore C.G.
      • Press N.
      • Au D.H.
      • Curtis J.R.
      • Wiener R.S.
      • Ganzini L.
      What the heck is a “nodule”? A qualitative study of veterans with pulmonary nodules.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      ‘The thing is not knowing': Patients' perspectives on surveillance of an indeterminate pulmonary nodule.
      Addressing these concerns has potential to improve both psychological and physical health outcomes, as high levels of cancer-related distress in other contexts have been associated with poor adherence with screening, evaluation, and treatment.
      • Taylor K.L.
      • Shelby R.
      • Gelmann E.
      • McGuire C.
      Quality of life and trial adherence among participants in the prostate, lung, colorectal, and ovarian cancer screening trial.
      • Dall'Era M.A.
      Patient and disease factors affecting the choice and adherence to active surveillance.
      • Hui S.K.
      • Miller S.M.
      • Wen K.Y.
      • et al.
      Psychosocial barriers to follow-up adherence after an abnormal cervical cytology test result among low-income, inner-city women.
      • Brett J.
      • Austoker J.
      Women who are recalled for further investigation for breast screening: psychological consequences 3 years after recall and factors affecting re-attendance.
      Encouragingly, a recent study by Slatore et al. suggests this distress may be able to be mitigated, as high-quality communication was associated with lower nodule-specific distress levels.
      • Slatore C.G.
      • Golden S.E.
      • Ganzini L.
      • Wiener R.S.
      • Au D.H.
      Distress and patient-centered communication among veterans with incidental (not screen-detected) pulmonary nodules. A cohort study.
      One critical misconception to rectify is the risk for cancer. We found no association between patients’ perceived risk for lung cancer and their estimated risk by the Mayo model, begging the question of why patients’ estimates of their cancer risk are so off base. One possibility, reported by 61% of patients in this survey, is that doctors are not providing information on cancer risk. Indeed, clinicians themselves have reported that they often do not supply information on cancer risk or even discuss cancer at all for fear of worrying patients with incidental nodules.
      • Golden S.E.
      • Wiener R.S.
      • Sullivan D.
      • Ganzini L.
      • Slatore C.G.
      Primary care providers and a system problem: a qualitative study of clinicians caring for patients with incidental pulmonary nodules.
      • Wiener R.S.
      • Slatore C.G.
      • Gillespie C.
      • Clark J.A.
      Pulmonologists' reported use of guidelines and shared decision-making in evaluation of pulmonary nodules: a qualitative study.
      However, those patients in our survey who reported receiving estimates of cancer risk more often found this information reassuring rather than scary, perhaps because the actual risk was much lower than the patients’ assumption of what their risk might be.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      What do you mean, a spot?: a qualitative analysis of patients' reactions to discussions with their physicians about pulmonary nodules.
      • Slatore C.G.
      • Press N.
      • Au D.H.
      • Curtis J.R.
      • Wiener R.S.
      • Ganzini L.
      What the heck is a “nodule”? A qualitative study of veterans with pulmonary nodules.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      ‘The thing is not knowing': Patients' perspectives on surveillance of an indeterminate pulmonary nodule.
      Another possibility however is that clinicians did provide information on cancer risk but patients were too overwhelmed by news of a nodule to process the information. This possibility is supported by prior work in the lung cancer screening setting suggesting that patients require repeated counseling on their estimated risk over the course of a year or more for this information to be fully absorbed.
      • Byrne M.M.
      • Weissfeld J.
      • Roberts M.S.
      Anxiety, fear of cancer, and perceived risk of cancer following lung cancer screening.
      Overall, patients in this study rated their physicians' communication skills highly, as is typical.
      • Little P.
      • Everitt H.
      • Williamson I.
      • et al.
      Observational study of effect of patient centredness and positive approach on outcomes of general practice consultations.
      However, deficits remained in conveying specific information about nodules that patients deem important.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      What do you mean, a spot?: a qualitative analysis of patients' reactions to discussions with their physicians about pulmonary nodules.
      • Slatore C.G.
      • Au D.H.
      • Press N.
      • Wiener R.S.
      • Golden S.E.
      • Ganzini L.
      Decision making among veterans with incidental pulmonary nodules: a qualitative analysis.
      • Slatore C.G.
      • Press N.
      • Au D.H.
      • Curtis J.R.
      • Wiener R.S.
      • Ganzini L.
      What the heck is a “nodule”? A qualitative study of veterans with pulmonary nodules.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      ‘The thing is not knowing': Patients' perspectives on surveillance of an indeterminate pulmonary nodule.
      • Slatore C.G.
      • Golden S.E.
      • Ganzini L.
      • Wiener R.S.
      • Au D.H.
      Distress and patient-centered communication among veterans with incidental (not screen-detected) pulmonary nodules. A cohort study.
      • Sullivan D.R.
      • Golden S.E.
      • Ganzini L.
      • Hansen L.
      • Slatore C.G.
      ‘I still don't know diddly': a longitudinal qualitative study of patients' knowledge and distress while undergoing evaluation of incidental pulmonary nodules.
      Our survey corroborates prior work
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      What do you mean, a spot?: a qualitative analysis of patients' reactions to discussions with their physicians about pulmonary nodules.
      • Wiener R.S.
      • Gould M.K.
      • Woloshin S.
      • Schwartz L.M.
      • Clark J.A.
      ‘The thing is not knowing': Patients' perspectives on surveillance of an indeterminate pulmonary nodule.
      • Slatore C.G.
      • Golden S.E.
      • Ganzini L.
      • Wiener R.S.
      • Au D.H.
      Distress and patient-centered communication among veterans with incidental (not screen-detected) pulmonary nodules. A cohort study.
      suggesting that certain nodule-specific communication strategies, such as reassuring patients that nodules are commonly found, indicating the size of the nodule, showing the CT scan, and sharing information on the risk for cancer, are well received by patients and tend to be more reassuring than anxiety provoking. Similarly, our study confirms that patients want to be involved in shared decision making about nodule evaluation far more than they typically are.
      • Slatore C.G.
      • Au D.H.
      • Press N.
      • Wiener R.S.
      • Golden S.E.
      • Ganzini L.
      Decision making among veterans with incidental pulmonary nodules: a qualitative analysis.
      • Golden S.E.
      • Wiener R.S.
      • Sullivan D.
      • Ganzini L.
      • Slatore C.G.
      Primary care providers and a system problem: a qualitative study of clinicians caring for patients with incidental pulmonary nodules.
      • Wiener R.S.
      • Slatore C.G.
      • Gillespie C.
      • Clark J.A.
      Pulmonologists' reported use of guidelines and shared decision-making in evaluation of pulmonary nodules: a qualitative study.
      The vast majority of patients were glad to know about the nodule. Indeed, nodule detection may have positive health effects. More than a third of our respondents (38%) reported that they quit smoking after the identification of a pulmonary nodule, although how each individual defined smoking cessation or whether this benefit persisted is unknown. This suggests that nodule detection may represent a “teachable moment” with regard to smoking cessation and is consistent with the finding that patients with a screen-detected nodule are more likely to quit smoking than are those with a normal screening CT result.
      • Tammemagi M.C.
      • Berg C.D.
      • Riley T.L.
      • Cunningham C.R.
      • Taylor K.L.
      Impact of lung cancer screening results on smoking cessation.
      • Ostroff J.S.
      • Buckshee N.
      • Mancuso C.A.
      • Yankelevitz D.F.
      • Henschke C.I.
      Smoking cessation following CT screening for early detection of lung cancer.
      • Slatore C.G.
      • Baumann C.
      • Pappas M.
      • Humphrey L.L.
      Smoking behaviors among patients receiving computed tomography for lung cancer screening. Systematic review in support of the U.S. Preventive Services Task Force.
      • Clark M.A.
      • Gorelick J.J.
      • Sicks J.D.
      • et al.
      The relations between false positive and negative screens and smoking cessation and relapse in the National Lung Cancer Screening Trial: implications for public health.
      This study has limitations. Only half of the surveyed individuals responded. If nonrespondents tended not to participate because of little interest in or concern over their pulmonary nodule, our results would be biased toward overstating the impact of nodule detection. This study did not collect the longitudinal data or detailed information about the timing of nodule detection needed to permit a clear picture of the trajectory of distress among patients with incidental nodules, and indeed, there may have been a higher peak of early distress (as observed in lung cancer screening trials) that we did not capture. Nonetheless, the fact that a quarter of patients experienced clinically significant distress regardless of time since nodule detection is notable. Because we purposefully selected sites that serve low-income populations and all these sites are located in the northeastern United States, our results may not be generalizable to all patients. For example, numeracy and literacy may be particularly low in our sample, and some of the observed misperception of cancer risk may reflect poor comprehension of survey items. Importantly, our findings among patients with incidentally detected nodules may or may not represent patients with screen-detected nodules. It is unknown whether patients undergoing screening in a “real world” setting will experience the same low levels of distress observed in clinical trials or the higher distress observed in this and other observational studies of patients with incidental nodules in usual practice. As called for in a recent statement of the American Thoracic Society,
      • Slatore C.G.
      • Horeweg N.
      • Jett J.R.
      • et al.
      An official American Thoracic Society research statement: a research framework for pulmonary nodule evaluation and management.
      studies examining distress as lung cancer screening is implemented into usual practice are urgently needed.
      With rising use of CT for a variety of indications, including for lung cancer screening, clinicians will increasingly be faced with the challenge of how to counsel patients when a pulmonary nodule is found. Our study shows that misconceptions and distress are common and that current smokers and those with economic hardships may be particularly susceptible to nodule-specific distress. Clinicians should be attentive to communication with patients about pulmonary nodules and consider using certain nodule-specific communication strategies, such as telling the patient the size of the nodule and the corresponding risk for cancer, showing the patient the CT, and discussing how commonly nodules are found. These simple communication strategies may help improve the experience of the hundreds of thousands of patients each year who are found to have a pulmonary nodule.

      Acknowledgments

      This work was funded by the National Institutes of Health (grant K07 CA 138772) and with resources from the Edith Nourse Rogers VA Memorial Hospital, Bedford, Massachusetts, and the VA Portland Healthcare System, Portland, Oregon. The funding organizations did not have a direct role in the design or conduct of the study, nor did it have a direct role in the collection, management, analysis, or interpretation of the data or in preparation, review, or approval of the manuscript. The views expressed in this manuscript do not necessarily represent the views of the Department of Veterans Affairs or the United States Government. Dr. Wiener had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. We would like to thank Ashley Wagner, BA, Emilie Zoltick, MPH, and Denise Clarke, MBA, who acted as research coordinators for this project and assisted in survey administration and data collection.

      Supplementary Data

      References

        • Aberle D.R.
        • Adams A.M.
        • et al.
        • National Lung Screening Trial Research Team
        Reduced lung-cancer mortality with low-dose computed tomographic screening.
        N Engl J Med. 2011; 365: 395-409
        • Gould M.K.
        • Tang T.
        • Liu I.A.
        • et al.
        Recent trends in the identification of incidental pulmonary nodules.
        Am J Respir Crit Care Med. 2015; 192: 1208-1214
        • Wiener R.S.
        • Gould M.K.
        • Woloshin S.
        • Schwartz L.M.
        • Clark J.A.
        What do you mean, a spot?: a qualitative analysis of patients' reactions to discussions with their physicians about pulmonary nodules.
        Chest. 2013; 143: 672-677
        • Gould M.K.
        • Fletcher J.
        • Iannettoni M.D.
        • et al.
        Evaluation of patients with pulmonary nodules: when is it lung cancer?: ACCP evidence-based clinical practice guidelines (2nd edition).
        Chest. 2007; 132: 108S-130S
        • MacMahon H.
        • Austin J.H.
        • Gamsu G.
        • et al.
        Guidelines for management of small pulmonary nodules detected on CT scans: a statement from the Fleischner Society.
        Radiology. 2005; 237: 395-400
        • Callister M.E.
        • Baldwin D.R.
        • Akram A.R.
        • et al.
        British thoracic society guidelines for the investigation and management of pulmonary nodules.
        Thorax. 2015; 70: ii1-ii54
        • Slatore C.G.
        • Au D.H.
        • Press N.
        • Wiener R.S.
        • Golden S.E.
        • Ganzini L.
        Decision making among veterans with incidental pulmonary nodules: a qualitative analysis.
        Respir Med. 2015; 109: 532-539
        • Slatore C.G.
        • Press N.
        • Au D.H.
        • Curtis J.R.
        • Wiener R.S.
        • Ganzini L.
        What the heck is a “nodule”? A qualitative study of veterans with pulmonary nodules.
        Ann Am Thorac Soc. 2013; 10: 330-335
        • Wiener R.S.
        • Gould M.K.
        • Woloshin S.
        • Schwartz L.M.
        • Clark J.A.
        ‘The thing is not knowing': Patients' perspectives on surveillance of an indeterminate pulmonary nodule.
        Health Expect. 2015; 18: 355-365
        • Slatore C.G.
        • Golden S.E.
        • Ganzini L.
        • Wiener R.S.
        • Au D.H.
        Distress and patient-centered communication among veterans with incidental (not screen-detected) pulmonary nodules. A cohort study.
        Ann Am Thorac Soc. 2015; 12: 184-192
        • Slatore C.G.
        • Horeweg N.
        • Jett J.R.
        • et al.
        An official American Thoracic Society research statement: a research framework for pulmonary nodule evaluation and management.
        Am J Respir Crit Care Med. 2015; 192: 500-514
        • Little P.
        • Everitt H.
        • Williamson I.
        • et al.
        Observational study of effect of patient centredness and positive approach on outcomes of general practice consultations.
        BMJ. 2001; 323: 908-911
        • Horowitz M.
        • Wilner N.
        • Alvarez W.
        Impact of event scale: a measure of subjective stress.
        Psychosom Med. 1979; 41: 209-218
        • Joseph S.
        Psychometric evaluation of Horowitz's Impact of Event Scale: a review.
        J Trauma Stress. 2000; 13: 101-113
        • van den Bergh K.A.
        • Essink-Bot M.L.
        • Borsboom G.J.
        • Scholten E.T.
        • van Klaveren R.J.
        • de Koning H.J.
        Long-term effects of lung cancer computed tomography screening on health-related quality of life: The NELSON trial.
        Eur Respir J. 2011; 38: 154-161
        • Taylor K.L.
        • Shelby R.
        • Gelmann E.
        • McGuire C.
        Quality of life and trial adherence among participants in the prostate, lung, colorectal, and ovarian cancer screening trial.
        J Natl Cancer Inst. 2004; 96: 1083-1094
        • Landsbergen K.M.
        • Prins J.B.
        • Brunner H.G.
        • Hoogerbrugge N.
        Shortened time interval between colorectal cancer diagnosis and risk testing for hereditary colorectal cancer is not related to higher psychological distress.
        Fam Cancer. 2011; 10: 51-57
        • Fiscella K.
        • Whitley E.
        • Hendren S.
        • et al.
        Patient navigation for breast and colorectal cancer treatment: a randomized trial.
        Cancer Epidemiol Biomarkers Prev. 2012; 21: 1673-1681
        • Shoma A.M.
        • Mohamed M.H.
        • Nouman N.
        • et al.
        Body image disturbance and surgical decision making in Egyptian post menopausal breast cancer patients.
        World J Surg Oncol. 2009; 7: 66
        • Butow P.N.
        • Fardell J.E.
        • Smith A.
        Fear of cancer recurrence: an overview and Australian perspective.
        Cancer Forum. August 2015; 39: 95
      1. Corcoran K. Fischer J. Measures for Clinical Practice and Research: A Sourcebook. 5th ed. Oxford University Press, Oxford, UK2013
        • Swensen S.J.
        • Silverstein M.D.
        • Ilstrup D.M.
        • Schleck C.D.
        • Edell E.S.
        The probability of malignancy in solitary pulmonary nodules. Application to small radiologically indeterminate nodules.
        Arch Intern Med. 1997; 157: 849-855
        • Hudon C.
        • Fortin M.
        • Haggerty J.L.
        • Lambert M.
        • Poitras M.E.
        Measuring patients' perceptions of patient-centered care: a systematic review of tools for family medicine.
        Ann Fam Med. 2011; 9: 155-164
        • Sullivan D.R.
        • Golden S.E.
        • Ganzini L.
        • Hansen L.
        • Slatore C.G.
        ‘I still don't know diddly': a longitudinal qualitative study of patients' knowledge and distress while undergoing evaluation of incidental pulmonary nodules.
        NPJ Prim Care Respir Med. 2015; 25: 15028
        • Lemonnier I.
        • Baumann C.
        • Jolly D.
        • et al.
        Solitary pulmonary nodules: consequences for patient quality of life.
        Qual Life Res. 2011; 20: 101-109
        • Gareen I.F.
        • Duan F.
        • Greco E.M.
        • et al.
        Impact of lung cancer screening results on participant health-related quality of life and state anxiety in the National Lung Screening Trial.
        Cancer. 2014; 120: 3401-3409
        • Kaerlev L.
        • Iachina M.
        • Pedersen J.H.
        • Green A.
        • Norgard B.M.
        CT-screening for lung cancer does not increase the use of anxiolytic or antidepressant medication.
        BMC Cancer. 2012; 12: 188
        • Slatore C.G.
        • Sullivan D.R.
        • Pappas M.
        • Humphrey L.L.
        Patient-centered outcomes among lung cancer screening recipients with computed tomography: a systematic review.
        J Thorac Oncol. 2014; 9: 927-934
        • Byrne M.M.
        • Weissfeld J.
        • Roberts M.S.
        Anxiety, fear of cancer, and perceived risk of cancer following lung cancer screening.
        Med Decis Making. 2008; 28: 917-925
        • Mazzone P.J.
        • Obuchowski N.
        • Fu A.Z.
        • Phillips M.
        • Meziane M.
        Quality of life and healthcare use in a randomized controlled lung cancer screening study.
        Ann Am Thorac Soc. 2013; 10: 324-329
        • Adler N.E.
        • Stead W.W.
        Patients in context—EHR capture of social and behavioral determinants of health.
        N Engl J Med. 2015; 372: 698-701
        • Franks P.
        • Tancredi D.J.
        • Winters P.
        • Fiscella K.
        Including socioeconomic status in coronary heart disease risk estimation.
        Ann Fam Med. 2010; 8: 447-453
        • Committee on the Recommended Social and Behavioral Domains and Measures for Electronic Health Records, Board on Population Health and Public Health Practice, Institute of Medicine
        Capturing Social and Behavioral Domains and Measures in Electronic Health Records: Phase 2.
        National Academies Press, Washington, DC2015
        • Walker R.J.
        • Smalls B.L.
        • Campbell J.A.
        • Strom Williams J.L.
        • Egede L.E.
        Impact of social determinants of health on outcomes for type 2 diabetes: a systematic review.
        Endocrine. 2014; 47: 29-48
        • Harris R.P.
        • Sheridan S.L.
        • Lewis C.L.
        • et al.
        The harms of screening: a proposed taxonomy and application to lung cancer screening.
        JAMA Intern Med. 2014; 174: 281-285
        • Jonnalagadda S.
        • Bergamo C.
        • Lin J.J.
        • et al.
        Beliefs and attitudes about lung cancer screening among smokers.
        Lung Cancer. 2012; 77: 526-531
        • Dall'Era M.A.
        Patient and disease factors affecting the choice and adherence to active surveillance.
        Curr Opin Urol. 2015; 25: 272-276
        • Hui S.K.
        • Miller S.M.
        • Wen K.Y.
        • et al.
        Psychosocial barriers to follow-up adherence after an abnormal cervical cytology test result among low-income, inner-city women.
        J Prim Care Community Health. 2014; 5: 234-241
        • Brett J.
        • Austoker J.
        Women who are recalled for further investigation for breast screening: psychological consequences 3 years after recall and factors affecting re-attendance.
        J Public Health Med. 2001; 23: 292-300
        • Golden S.E.
        • Wiener R.S.
        • Sullivan D.
        • Ganzini L.
        • Slatore C.G.
        Primary care providers and a system problem: a qualitative study of clinicians caring for patients with incidental pulmonary nodules.
        Chest. 2015; 148: 1422-1429
        • Wiener R.S.
        • Slatore C.G.
        • Gillespie C.
        • Clark J.A.
        Pulmonologists' reported use of guidelines and shared decision-making in evaluation of pulmonary nodules: a qualitative study.
        Chest. 2015; 148: 1415-1421
        • Tammemagi M.C.
        • Berg C.D.
        • Riley T.L.
        • Cunningham C.R.
        • Taylor K.L.
        Impact of lung cancer screening results on smoking cessation.
        J Natl Cancer Inst. 2014; 106: dju084
        • Ostroff J.S.
        • Buckshee N.
        • Mancuso C.A.
        • Yankelevitz D.F.
        • Henschke C.I.
        Smoking cessation following CT screening for early detection of lung cancer.
        Prev Med. 2001; 33: 613-621
        • Slatore C.G.
        • Baumann C.
        • Pappas M.
        • Humphrey L.L.
        Smoking behaviors among patients receiving computed tomography for lung cancer screening. Systematic review in support of the U.S. Preventive Services Task Force.
        Ann Am Thorac Soc. 2014; 11: 619-627
        • Clark M.A.
        • Gorelick J.J.
        • Sicks J.D.
        • et al.
        The relations between false positive and negative screens and smoking cessation and relapse in the National Lung Cancer Screening Trial: implications for public health.
        Nicotine Tob Res. 2015; 18: 17-24