Impact of a Lung Cancer Screening Counseling and Shared Decision-Making Visit

Accepted Manuscript Impact of a Lung Cancer Screening Counseling and Shared-Decision-Making Visit Peter J. Mazzone, MD, MPH, FCCP, Amanda Tenenbaum, CNP, Meredith Seeley, BSS, Hilary Petersen, PA, Christina Lyon, Xiaozhen Han, MS, Xiao-Feng Wang, PhD PII:

S0012-3692(16)62293-6

DOI:

10.1016/j.chest.2016.10.027

Reference:

CHEST 772

To appear in:

CHEST

Received Date: 11 August 2016 Revised Date:

5 October 2016

Accepted Date: 17 October 2016

Please cite this article as: Mazzone PJ, Tenenbaum A, Seeley M, Petersen H, Lyon C, Han X, Wang XF, Impact of a Lung Cancer Screening Counseling and Shared-Decision-Making Visit, CHEST (2016), doi: 10.1016/j.chest.2016.10.027. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Word Counts: Abstract 245, Text 2775 Impact of a Lung Cancer Screening Counseling and Shared-Decision-Making Visit Peter J Mazzone MD, MPH, FCCP, Amanda Tenenbaum CNP, Meredith Seeley BSS, Hilary Petersen PA, Christina Lyon, Xiaozhen Han MS, Xiao-Feng Wang PhD

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Respiratory Institute, Cleveland Clinic Corresponding Author Peter J Mazzone 9500 Euclid Ave, A90

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Cleveland, OH 44195

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[email protected]

No conflicts of interest exist for any author related to the content of this manuscript PJM takes responsibility for the integrity of the data and the accuracy of the data analysis. PJM assumes full responsibility for the integrity of the submission as a whole, from inception to published article. Abbreviations

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CT – computed tomography, EMR – electronic medical record, LDCT – low radiation dose chest computed tomography

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Abstract Background: Lung cancer screening is a complex balance of benefit and harms. A counseling and shared decision making visit has been mandated to assist patient’s with the decision about participation in screening. The impact of this visit on patient understanding and decisions has not been studied.

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Methods: We developed a centralized counseling and shared decision making visit for our lung cancer screening program. The visit included confirmation of eligibility for screening, education supported by a narrated slide show, individualized risk assessment with a decision-aid, time for answering questions and data collection. We surveyed consecutive patients prior to their visit, immediately after their visit, and 1-month after their visit to determine the impact of the visit on their knowledge.

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Results: 23 of 423 (5.4%) patients who had a visit did not proceed on to the screening CT scan. 125 consecutive patients completed the initial survey, 122 the post-visit survey, and 113 the 1-month followup survey. Prior to the visit the patients had a poor level of understanding about the age and smoking eligibility criteria (8.8% and 13.6% correct respectively), and the benefit and harms of screening (55.2% and 38.4% correct respectively). There was a significant improvement in knowledge noted after the visit for all questions (p=0.03 – p<0.0001). Knowledge waned by the 1-month follow-up but remained higher than it was pre-visit.

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Conclusions: A centralized counseling and shared decision making visit impacts knowledge of the eligibility criteria, benefit, and harms of lung cancer screening with LDCT, helping patients make value based decisions.

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Introduction

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Lung cancer screening with a low radiation dose chest CT scan (LDCT) has been recommended by most stakeholder societies based on evidence that the benefit of screening outweighs the harms1-6. These recommendations recognize that the favorable balance is tenuous, and tied to the quality of implementation of screening7. Screening presents a unique challenge to this balance as a minority of patients screened will experience the benefit while all have the potential to be harmed, and all patients are presumably healthy at the time of screening. In addition, the fulcrum of this balance shifts based on how an individual patient values each side of the balance.

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Given the tenuous balance and unequal value of benefit and harms, it is important that patient’s share in the decision about whether or not to pursue lung cancer screening. In order to share in the decision and express their values, a patient must be fully informed about the background, expectations, and alternatives to lung cancer screening.

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Shared decision making has been defined as a “collaborative process that allows patients and their health care providers to make health care decisions together, taking into account the best scientific evidence available, as well as the patient’s values and preferences”. This process has a goal of giving patients the support needed to make individualized decisions8,9. For the purpose of lung cancer screening, the Center for Medicare and Medicaid Services has mandated a lung cancer screening counseling and shared decision making visit10.

Materials and Methods

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To our knowledge the impact of the counseling and shared decision making visit on a patients’ understanding of the benefit and harms of screening, their interest in participating in lung cancer screening, and the program’s ability to insure patient’s meet eligibility criteria, has not been described. We designed a counseling and shared decision making visit for our lung cancer screening program and describe its impact in this report.

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From April 1st 2015 onward we performed face to face counseling and shared decision making visits with patients referred to our lung cancer screening program. Patients were identified as potentially eligible for screening by their primary care or specialty provider. The screening program reviewed the patient’s electronic medical record (EMR) to confirm they met screening program eligibility criteria. All eligible patients were scheduled for their counseling and shared decision making visit with a LDCT coordinated after the visit. The counseling and shared decision making visits were usually staffed by a nurse practitioner (AT), and less often by a physician assistant (HP) or physician (PM). The counseling and shared decision making visit began with a review of patient eligibility criteria. This was followed by the presentation of an approximately 6-minute narrated video slide show, developed by our program, describing the benefit and harms of lung cancer screening; the use of a decision aid (shouldiscreen.com) to individualize the discussion of benefit and risk; and data collection. Patients had an opportunity to ask questions throughout the visit, including a prompt for questions from the provider at the end of the video slide show. The project was approved by the Institutional Review Board of the Cleveland Clinic as a quality assessment and improvement activity. Consecutive patients were approached from 11/18/2015 through 3/1/2016 to complete surveys with a goal of enrolling 125 patients in hopes that at least 100 would

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complete responses at all three survey time points. Surveys were administered in-person immediately prior to and immediately after the visit. A final survey was administered by telephone approximately one month after the visit was completed. The following questions were asked. Pre-visit survey

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1. What age range must you be in to qualify for lung cancer screening? (Correct defined as age 55 to 74 through 80) 2. How much cigarette smoking must you have done in your life to qualify for lung cancer screening? (Correct defined as ≥ 30 pack-years, Partially correct as 30 pack-years) 3. What is the potential benefit of lung cancer screening? (Correct defined as fewer people dying from lung cancer, Partially correct as early detection of lung cancer, and Partially correct 2 as detection of lung cancer) 4. List one potential harm of lung cancer screening. (Correct included finding lung nodules, procedures and testing for benign disease, anxiety or distress related to test findings, radiation exposure and its potential consequences, overdiagnosis) Immediate post-visit survey

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1. What age range must you be in to qualify for lung cancer screening? 2. How much cigarette smoking must you have done in your life to qualify for lung cancer screening? 3. What is the potential benefit of lung cancer screening? 4. Was the information about the benefit of lung cancer screening presented with an appropriate level of detail (scale of 1 to 5 with 3 = at my level, 1 = much too simple, 5 = much too difficult)? 5. List one potential harm of lung cancer screening. 6. Was the information about the harms of lung cancer screening presented with an appropriate level of detail (scale of 1 to 5 with 3 = appropriate, 1 = much too simple, 5 = much too difficult)? 7. Was the information about the balance of benefit to harms of lung cancer screening presented with an appropriate level of detail (scale of 1 to 5 with 3 = appropriate, 1 = much too simple, 5 = much too difficult)? 8. Did the information about your individual risk of developing lung cancer help you decide whether you should participate in lung cancer screening (scale of 1 to 5 with 3 = no help, 1 = made me less comfortable, 5 = made me more comfortable)? 9. Comments about the presentation and visit: 1 month post visit survey

1. What age range must you be in to qualify for lung cancer screening? 2. How much cigarette smoking must you have done in your life to qualify for lung cancer screening? 3. What is the potential benefit of lung cancer screening? 4. List one potential harm of lung cancer screening.

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COPD was defined as a clinical diagnosis in the EMR and confirmed by the patient during the visit. Summaries of patient responses and education levels were described using counts and percentages for all categorical variables. To test for differences in responses between the survey times both the Bhapkar test and Stuart Maxwell test were performed. Poisson regression analysis was performed to evaluate the interaction of education level and survey time on patient responses. All analyses were two-tailed and were performed at a significance level of 0.05. SAS 9.3 software (SAS Institute, Cary, NC) was used for all analyses. The SAS macro for the Bhapkar test and Stuart Maxwell test is developed by Keith Dunnigan11. Results

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423 patients had a shared decision making visit between 4/2015 and 4/2016. Of these, 23 (5.4%) patients did not go on to have the LDCT exam. 11 of the 23 chose not to proceed after completing the visit. 9 of the 23 did not meet our criteria for screening (7 by smoking history, 1 by age, 1 had a CT within the past 12 months), and 3 were symptomatic (2 weight loss, 1 chest pain). 125 patients completed the pre-visit survey, 122 the post-visit survey, and 113 the one month post-visit survey. The patients were a mean age of 64.4 years (range 55-77), 33.9% were women, 45.2% were active smokers, the mean packyears smoked was 53.0 (range 30-112), and 40.3% had chronic obstructive pulmonary disease. 11 (8.9%) did not complete high school, 36 (29.0%) were high school graduates, 31 (25.0%) attended some college, 28 (22.6%) were college graduates, and 16 (12.9%) completed post-graduate education.

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Age criteria: Prior to the visit, 24 patients (19.2%) stated they did not know, and 12 (9.6%) stated any age. In total, 11 (8.8%) were correct, 112 (89.6%) were incorrect, and 2 (1.6%) did not respond. Knowledge improved immediately after the visit with 3 (2.4%) stating they did not known, and 1 (0.8%) stating any age. In total, 74 (59.2%) were correct, 48 (38.4%) were incorrect, and 3 (2.4%) did not respond. Knowledge waned over time but remained better than prior to the visit. At the one-month follow-up survey 15 (12.1%) stated they did not know, 2 (1.6%) stated any age, and 12 did not respond (9.7%). Of the responders 24 (21.4%) were correct, and 88 were incorrect (78.6%) (Figure 1a, Table 1).

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Smoking criteria: Prior to the visit, 17 (13.6%) were correct and 14 (11.2%) partially correct. After the visit, knowledge improved with 51 (40.8%) correct and 25 (20%) partially correct. Much of the knowledge improvement persisted to the 1-month post visit survey with 44 (35.5%) correct and 10 (8.1%) partially correct (Figure 1b, Table 1).

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Benefit and Harms: Using a liberal definition of benefit (finding early lung cancer, or fewer people dying of lung cancer), 69 (55.2%) were correct prior to the visit, 81 (66.4%) were correct after the visit, and 66 (58.8%) were correct at the one-month follow-up. Using a more restrictive definition of benefit (fewer people dying of lung cancer) there was a poor level of knowledge at all time points (4.8%, 8.0%, and 3.2% correct before, immediately after, and 1-month after respectively). There was a more substantial improvement in knowledge about the harms of screening, with 77 (61.6%) unable to identify one potential harm prior to the visit, 12 (9.6%) immediately after the visit, and 24 (21.4%) at the one month follow-up (Figure 1c and 1d, Table 1). A significant difference in the distribution of responses by level education was present prior to the visit for the questions about the smoking criteria for eligibility (p=0.016), and the potential harms of screening (p=0.021). Differences in the distribution of responses were present after the visit for the questions about the smoking criteria (p=0.029), knowledge of the benefit (p=0.041), and knowledge of

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the harms (p=0.019). Differences in the distribution of responses were present at the 1-month follow-up time for the questions about the smoking criteria (p=0.049) and knowledge of harms (0.003). Those with the lowest level of formal education were more likely to provide incorrect answers at all time-points (Table 2). The improvement in knowledge from the visit was equal across the levels of formal education (p=0.22-0.97).

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The patient’s assessment of the appropriateness of the presentation of benefit (mean 2.92 +/- 0.79), harms (mean 2.97, +/- 0.77), and the balance of benefit and harms (mean 3.01, +/- 0.78) suggest that they felt the messages were delivered at an appropriate level (3 = at my level). Information about the individual risk-benefit balance helped patients feel more comfortable about their decision (mean 3.88 +/- 1.29; 5 = made me more comfortable). Of the 66 patients who provided comments about the visit, 57 were positive (e.g. “good presentation helped me to make an informed choice”, “Excellent! No unnecessary pressure – honest, highly intelligent and sensitive to needs of my whole life”), and 9 were negative (e.g. “information regarding harm of screening is confusing”, “boring”).

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Discussion

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This project had a goal of determining the impact of a lung cancer screening counseling and shared decision making visit on patient understanding of the benefit and harms of screening, and their decision about whether or not to complete the screening exam. We found a small but not insignificant portion of patients (5.4%) did not proceed on to the screening exam, either because of ineligibility or choice. We also found a generally poor level of understanding of the eligibility criteria, benefit, and harms of screening upon entry into the program. This understanding improved substantially after the visit, at the time of the decision about whether or not to proceed with screening. The knowledge gained was partly lost by one-month after the visit. Patients generally felt the messages were delivered at an appropriate level and felt more comfortable about their decision after the visit. Finally, those with the lowest level of formal education appeared to have less knowledge about screening at baseline and after the visit.

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In order for a patient to make a value based judgment about whether to proceed with screening they need to have a level of understanding of the benefit and harms that allows them to participate in the decision. Our results suggest that the majority of patients did not have an adequate level of understanding prior to the visit. Most patients did not know the eligibility criteria for lung cancer screening. They had a better understanding of the potential benefit of screening than the harms. This is compatible with a previous evaluation of informed decision making for colorectal, breast, and prostate cancer screening. Patients in that study reported that over 90% of providers discussed the benefit of screening, while only 19-30% discussed the potential harms of screening.12 It is possible that the ordering providers in our study were more comfortable in discussing the benefit of screening. Our patients’ understanding of both the benefit and harms improved immediately after the visit. A minority of the patients in our group gave incorrect answers about the benefit of screening (13.6%) and harms of screening (9.6%) immediately after the visit, at the time they were making a decision about whether or not to proceed with screening. The population eligible for screening is heterogeneous in age, race, co-morbid conditions, and education level. These factors influence the benefit and harms of screening, as well as the willingness of an individual to participate in screening13-16. Delivery of information in a standardized format may lead to different outcomes for subgroups of this population. Our visit was designed to have standardized elements, but also to individualize discussion while providing time for questions and answers in an effort

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to minimize the influence of these variables on the success of the visit. Our patient population had a similar education level to the NLST participants (8.9% did not complete high school in our study, 6.1% in the NLST; 35.5% had a college degree or higher in our study, 31.5% in the NLST)17, which is known to be higher than the general population of eligible individuals (21.3% with less than high school level education, 12.9-14.4% with a college degree or higher)17,18. This could impact the generalizability of our findings. Our data suggests that those with the lowest level of formal education had the poorest understanding at all time-points, but that the benefit from the visit was equal across all levels of education. Strategies to enhance the education of those with the lowest education levels should be further explored.

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In other settings, research has shown that primary care providers and pulmonologists may not have the understanding, comfort level, or time to engage patients in shared decision making19-21. Our pre-visit survey suggests that any counseling that occurred prior to the visit was either ineffective or the benefit was transient. Since the patients had a better understanding of the benefit than harms of screening, it is possible that the ordering provider was more comfortable in discussing the benefit of screening. Our findings demonstrate that knowledge gained during the visit wanes over time, suggesting additional value to a shared decision making visit prior to each annual screen. This would also provide an opportunity to re-confirm eligibility, deliver additional smoking cessation counseling when needed, and build a patient-provider relationship. Information about personalized risk has been shown to help patients make more informed choices about participation in screening for other cancers22,23. This portion of our visit may have contributed to the increased level of comfort with the decision to pursue lung cancer screening expressed by our patients.

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There are limitations to our study. Our patients were referred from their primary care or subspecialty provider and eligibility was assessed by the program through a review of the EMR prior to the visit. Our results could have been more pronounced had these steps not occurred. Patients who select screening are often more interested in preventive health and healthier at baseline24. Thus, these results may not reflect the impact of a visit with all eligible patients. We used a liberal definition of the benefit of screening and only asked for one potential harm from screening.

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The strengths of our study include a reasonable number of participants of variable backgrounds and very good retention of patients at all time-points. The results are consistent and significant enough to suggest they are robust. Future research might address patient satisfaction with their decisions, assessment of the individual components of visit, the impact of the visit on compliance with follow-up and smoking cessation, and the added value of an annual SDM visit. Conclusions

A centralized counseling and shared decision making visit appears to impact knowledge of the eligibility criteria, benefit, and harms of lung cancer screening with LDCT. The visit was capable of helping patients across a spectrum of education levels make value based decisions. Acknowledgments PJM takes responsibility for the integrity of the data and the accuracy of the data analysis. PJM assumes full responsibility for the integrity of the submission as a whole, from inception to published article. AT, HP, MS, and CL made substantial contribution to the study design, data collection and interpretation,

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and the writing of the manuscript. XW and XH made substantial contribution to the study design, data analysis and interpretation, and the writing of the manuscript. References

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1. Bach PB, Mirkin JN, Oliver TK, et al. Benefits and harms of CT screening for lung cancer: a systematic review. JAMA. 2012;307(22):2418-2429. 2. Wender R, Fontham ETH, Barrera E, et al. American Cancer Society lung cancer screening guidelines. CA Cancer J Clin. 2013;63(2):106-117. 3. Detterbeck FC, Mazzone PJ, Naidich DF, Bach PB. Screening for lung cancer. Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest. 2013;143(5 suppl):e78S-e92S. 4. http://www.lung.org/assets/documents/lung-cancer/lung-cancer-screening-report.pdf. Accessed July 13th, 2016. 5. https://www.nccn.org/professionals/physician_gls/pdf/lung_screening.pdf. Accessed July 13th, 2016. 6. Moyer VA. US Preventive Services Task Force. Screening for lung cancer: US Preventive Services Task Force recommendation statement. Ann Intern Med. 2014;160(5):330-338. 7. Mazzone P, Powell CA, Arenberg D, et al. Components necessary for high-quality lung cancer screening: American College of Chest Physicians and American Thoracic Society Policy Statement. Chest. 2015;147(2):295-303. 8. http://www.informedmedicaldecisions.org/shareddecisionmaking.aspx. Accessed July 13th, 2016. 9. Volk RJ, Llewellyn-Thomas H, Stacey D, Bwyn G. Ten years of the International Patient Decision Aid Standards Collaboration: evolution of the core dimensions for assessing the quality of patient decision aids. BMC Med Informatics Decision Making. 2013;13(Suppl 2):S1, http://www.biomedcentral.com/1472-6947/13/S2/S1. 10. https://www.cms.gov/medicare-coverage-database/details/nca-decisionmemo.aspx?NCAId=274. Accessed July 13th, 2016. 11. Dunnigan K. Tests of marginal homogeneity and special cases. Pharmaceut Statist. 2013;12:213– 216. doi: 10.1002/pst.1573. 12. Hoffman RM, Lewis CL, Pignone M, et al. Decision-making processes for breast, colorectal, and prostate cancer screening: results from the DECISIONS study. Med Decis Making 2010;30(5 Suppl):53S-64S. 13. Tanner NT, Gebregziabher M, Halbert CH, Payne E, Egede LE, Silverstri GA. Racial differences in outcomes within the National Lung Screening Trial. Implications for widespread implementation. Am J Respir Crit Care Med. 2015;192(2):200-208. 14. Silvestri GA, Nietert PJ, Zoller J, Carter C, Bradford D. Attitudes towards screening for lung cancer among smokers and their non-smoking counterparts. Thorax. 2007;62(2):126-130. 15. Dominioni L, Rotolo N, Poli A, et al. Self-selection effects in smokers attending lung cancer screening: a 9.5-year population-based cohort study in Varese, Italy. J Thorac Oncol. 2010;5(4):428-435.

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16. Pinsky PF, Church TR, Izmirlian G, Kramer BS. The National Lung Screening Trial: Results stratified by demographics, smoking history, and lung cancer histology. Cancer. 2013;119:3976-3983. 17. Aberle DR, Adams AM, Berg CD, et al. Baseline characteristics of participants in the randomized National Lung Screening Trial. J Natl Cancer Inst 2010;102(23):1771-1779. 18. Howard DH, Richards TB, Bach PB, Kegler MC, Berg CJ. Comorbidities, smoking status, and life expectancy among individuals eligible for lung cancer screening. Cancer 2015;121(24):43414347. 19. Golden SE, Wiener RS, Sullivan D, Ganzini L, Slatore CG. Primary care providers and a system problem. A qualitative study of clinicians caring for patients with incidental pulmonary nodules. Chest. 2015;148(6):1422-1429. 20. Iaccarino JM, Clark J, Bolton R, et al. A national survey of Pulmonologists’ views on low-dose computed tomography screening for lung cancer. Ann Am Thorac Soc 2015;12(11):1667-1675. 21. Wiener RS, Slatore CG, Gillespie C, Clark JA. Pulmonologists’ reported use of guidelines and shared decision-making in evaluation of pulmonary nodules. A qualitative study. Chest. 2015;148(6):1415-1421. 22. Edwards AGK, Naik G, Ahmed H, et al. Personalised risk communication for informed decision making about taking screening tests. Cochrane Database Syst Rev 2013;2:CD001865. 23. Smith SK, Trevena L, Simpson JM, Barratt A, Nutbeam D, McCaffery KJ. A decision aid to support informed choices about bowel cancer screening among adults with low education: randomized controlled trial. BMJ 2010;341:c5370. 24. Yousaf-Khan U, Horeweg N, van der Aalst C, ten Haaf K, Oudkerk M, de Koning H. Baseline characteristics and mortality outcomes of control group participants and eligible nonresponders in the NELSON lung cancer screening study. J Thorac Oncol. 2015;10:747-753.

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Tables

HS (N=36)

Pre Post 1 month

100 45.5 72.7

88.9 41.7 75.0

Pre Post 1 month

100 54.5 54.5

75.0 44.4 52.8

Pre Post 1 month

45.5 0 27.3

Age

100 36.4 72.7

p-value

87.5 43.8 87.5

0.8738 0.2545 0.1289

80.6 38.7 64.5

64.3 21.4 17.9

62.5 37.5 50.0

0.0162 0.0292 0.0490

33.3 19.4 13.9

32.3 19.4 12.9

17.9 10.7 7.1

12.5 6.3 12.5

0.0812 0.0408 0.4541

69.4 11.1 19.4

54.8 6.5 19.4

50.0 3.6 7.1

50.0 6.3 6.3

0.0207 0.0187 0.0027

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Pre Post 1 month

PG (N=16)

82.1 35.7 60.7

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Harms

CG (N=28)

93.5 35.5 71.0

Smoking

Benefit

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Pre-Post Pre-1 month Post-1 month Age <0.0001 0.01 <0.0001 Smoking <0.0001 <0.0001 0.006 Benefit 0.03 0.09 0.45 Harms <0.0001 <0.0001 0.008 Table 1: Statistical significance of the comparison of survey responses for the four questions. Age = knowledge of screen-eligible ages; Smoking = knowledge of smoking history eligibility criteria; Benefit = knowledge of the benefit of lung cancer screening; Harms = knowledge of one potential harm from lung cancer screening; Pre = prior to the visit; Post = immediately after the visit; 1 month = 1 month after the visit.

Table 2: % of the survey responses that were incorrect for each of the survey questions, at each time point, separated by level of education.
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Figure Legend

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Figure 1: Change in knowledge from pre-visit, to immediately post visit, and one-month post visit for the four survey questions – 1a: Age eligibility criteria, 1b: Smoking eligibility criteria, 1c: Benefit of lung cancer screening, 1d: Harms of lung cancer screening.

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Change in Knowledge – Age Range 100

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80 70 60 50

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40 30 20 10 0

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Pre

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% of Responses

90

Incomplete

Figure 1a.

Post

Incorrect

1 mo Post

Correct

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Change in Knowledge – Smoking 80

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60 50 40 30

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% of Responses

70

20

0

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Pre

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10

Incomplete

Figure 1b.

Incorrect

Post Partially Correct

1 mo Post Correct

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100 90 80 70 60 50 40 30 20 10 0

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% of Responses

Change in Knowledge – Benefit

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Pre Incomplete

Figure 1c.

Incorrect

Post

Partially Correct

1 mo Post Partially Correct 2

Correct

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Change in Knowledge – Harms

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90 80 60 50

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40 30 20 10 0

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Pre

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% of Responses

70

Incomplete

Figure 1d.

Post Incorrect

1 mo Post Correct