National Prostate Cancer Screening Rates After the 2012 US Preventive Services Task Force Recommendation Discouraging Prostate-Specific Antigen-Based Screening.

Published Ahead of Print on June 8, 2015 as 10.1200/JCO.2015.61.6532 The latest version is at http://jco.ascopubs.org/cgi/doi/10.1200/JCO.2015.61.6532

JOURNAL OF CLINICAL ONCOLOGY

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National Prostate Cancer Screening Rates After the 2012 US Preventive Services Task Force Recommendation Discouraging Prostate-Specific Antigen–Based Screening Michael W. Drazer, Dezheng Huo, and Scott E. Eggener All authors: University of Chicago Medical Center, Chicago, IL. Published online ahead of print at www.jco.org on June 8, 2015. Processed as a Rapid Communication manuscript. Presented at the 51st Annual Meeting of the American Society of Clinical Oncology, Chicago, IL, May 29-June 2, 2015. Terms in blue are defined in the glossary, found at the end of this article and online at www.jco.org. Authors’ disclosures of potential conflicts of interest are found in the article online at www.jco.org. Author contributions are found at the end of this article. Corresponding author: Scott E. Eggener, MD, 5841 South Maryland, Mail Code 6038, University of Chicago Medical Center, Chicago, IL 60637; e-mail: [email protected] .edu. © 2015 by American Society of Clinical Oncology 0732-183X/15/3399-1/$20.00

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Purpose In 2012, the US Preventive Services Task Force (USPSTF) discouraged prostate-specific antigen (PSA) – based prostate cancer screening. Previous USPSTF recommendations did not appreciably alter prostate cancer screening. Therefore, we designed a trend analysis to determine the population-based impact of the 2012 recommendation. Methods The nationally representative National Health Interview Survey was used to estimate the proportion of men age 40 years and older who saw a physician and were screened for prostate cancer in 2013. An externally validated 9-year mortality index was used to analyze screening rates based on remaining life expectancy. Screening rates from 2005, 2010, and 2013 were compared using logistic regression. Results PSA-based screening did not significantly change from 2010 to 2013 among 40- to 49-year-old men (from 12.5% to 11.2%; P ⫽ .4). Screening rates significantly declined in men age 50 to 59 years (from 33.2% to 24.8%; P ⬍ .01), age 60 to 74 years (from 51.2% to 43.6%; P ⬍ .01), and age 75 years or older (from 43.9% to 37.1%; P ⫽ .03). A large percentage of men were screened for prostate cancer despite a high risk (⬎ 52%) of 9-year mortality, including approximately one third of men older than age 75 years. Approximately 1.4 million men age 65 years or older with a high risk (⬎ 52%) of 9-year mortality were screened in 2013. Conclusion Prostate cancer screening significantly declined among men older than age 50 years after the 2012 USPSTF guideline discouraging PSA-based screening. A significant proportion of men continue to be screened despite a high risk of 9-year mortality, including one third of men age 75 years and older.

DOI: 10.1200/JCO.2015.61.6532

J Clin Oncol 33. © 2015 by American Society of Clinical Oncology

INTRODUCTION

The debate over prostate-specific antigen (PSA)– based prostate cancer screening intensified after two randomized screening trials reported conflicting results on prostate cancer–specific mortality.1,2 The tenor of the controversy heightened after the 2012 US Preventive Services Task Force (USPSTF) recommendation discouraging PSA screening for asymptomatic men.3 That recommendation differed from guidelines published by the American Cancer Society and the American Urological Association, both of which endorsed consideration of screening based on age and estimated remaining life expectancy.4,5 Although many organizations publish cancer screening recommendations, primary care physi-

cians in the United States have cited the USPSTF as the most influential.3-10 Despite this, we demonstrated that a large proportion of men in the United States are screened for prostate cancer even without meeting criteria defined by the USPSTF and other organizations. For example, guidelines have encouraged physicians to only engage in shared decision making with men who have at least 10 years of remaining life expectancy.4-8 Yet, the prostate cancer screening rate among men age 70 years or older with a greater than 48% probability of 5-year mortality was 31% in 2005, representing approximately 777,000 men screened despite a high risk for overdiagnosis and overtreatment.11 In addition, screening rates among men age 65 years and older with a high (⬎ 52%) likelihood of 9-year mortality did not differ before and after the 2008 USPSTF recommendation, © 2015 by American Society of Clinical Oncology

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Drazer, Huo, and Eggener

despite that recommendation’s emphasis on limiting screening to men with at least 10 years of remaining life expectancy.12 Similarly, the 2008 USPSTF guidelines discouraging screening in men older than age 75 years did not appreciably alter screening rates.13 Given the public health implications, we conducted a populationbased trend analysis to determine the effects of the highly publicized 2012 USPSTF recommendation discouraging prostate cancer screening. Widespread national and social media coverage followed the initial release of the recommendation in October 2011.14-19 We used a large, nationally representative survey, the National Health Interview Survey (NHIS), to investigate three questions regarding prostate cancer screening. First, we estimated the proportion of men age 40 years and older screened in 2013. Second, we used an externally validated 9-year mortality index to analyze screening rates based on estimated remaining life expectancy.20 Finally, we compared screening rates in 2005, 2010, and 2013 to identify changes in national-level screening. All analyses were limited to men who saw a physician in the year before the survey.

METHODS Data Source and Participants This study was exempt from institutional review board review. The NHIS is a face-to-face, computer-assisted, cross-sectional survey performed on a rolling, annual basis in the United States. It is one of the major data collection programs from the Centers for Disease Control and Prevention and excludes active-duty military personnel as well as citizens residing in nursing homes, long-term care facilities, or correctional facilities. The survey oversamples minorities, and a single individual is unlikely to be sampled in multiple years. Employees from the US Census Bureau administer the survey, and results are released with sample weights based on population data. These weights may be used to extrapolate results to the US population.21 The NHIS typically releases cancer screening data every 5 years. The 2013 release, however, contained data regarding prostate cancer screening.21 We extracted data from the 2005, 2010, and 2013 NHIS databases for this study. We included men age 40 years and older and excluded men with a history of prostate cancer. We excluded men who did not know what a PSA test was or who had not seen a physician in the year before the survey. The NHIS asked all

Table 1. Characteristics of All Men Older Than Age 40 Years in the National Health Interview Survey No. of Respondents (%) Characteristic Race/ethnicity Non-Hispanic white Non-Hispanic black Hispanic Asian Other Highest education level Some high school High school diploma Some college College degree Marital status Not married Married/living with partner Colonoscopy history Never had colonoscopy Colonoscopy longer than 10 years ago Colonoscopy within last 10 years Body mass index Underweight/normal Overweight Obese Tobacco use Never smoker Former smoker Current smoker Personal cancer history No personal history of cancer Personal history of cancer Self-reported personal health status Excellent/very good Good Fair/poor 9-year predicted mortality riskⴱ Low risk High risk ⴱ

2

2005 Survey (n ⫽ 8,490)

2010 Survey (n ⫽ 7,326)

2013 Survey (n ⫽ 9,803)

6,045 (77.1) 1,022 (9.3) 1,073 (9.1) 236 (3.2) 114 (1.3)

4,548 (73.8) 1,152 (9.7) 1,110 (11.2) 410 (4.1) 106 (1.2)

6,424 (72.0) 1,353 (9.7) 1,326 (11.9) 505 (4.8) 195 (1.5)

1,558 (15.9) 2,434 (29.9) 2,072 (24.8) 2,328 (29.4)

1,359 (15.2) 1,997 (27.5) 1,869 (25.9) 2,061 (31.4)

1,702 (14.5) 2,579 (25.8) 2,587 (27.0) 2,886 (32.8)

3,149 (23.9) 5,290 (76.1)

2,894 (26.2) 4,419 (73.8)

4,040 (27.4) 5,738 (72.6)

4,930 (77.9) 162 (2.5) 1,272 (19.6)

3,746 (69.2) 171 (3.1) 1,451 (27.7)

5,137 (69.0) 299 (4.0) 2,057 (27.0)

2,344 (26.9) 3,766 (45.7) 2,154 (27.5)

1,888 (24.7) 3,145 (44.4) 2,152 (30.9)

2,418 (23.9) 4,224 (44.1) 2,997 (32.1)

3,653 (44.5) 2,884 (34.3) 1,861 (21.2)

3,373 (47.1) 2,402 (33.6) 1,491 (19.3)

4,561 (48.0) 3,293 (33.4) 1,904 (18.6)

7,835 (92.7) 645 (7.3)

6,718 (91.9) 598 (8.1)

8,956 (91.9) 835 (8.1)

4,429 (54.7) 2,512 (29.0) 1,542 (16.3)

3,696 (54.2) 2,236 (29.1) 1,391 (16.7)

4,970 (53.2) 2,894 (29.2) 1,936 (17.6)

1,531 (65.8) 853 (34.2)

1,352 (65.0) 787 (35.0)

2,047 (67.8) 1,068 (32.2)

Only for men age 65 years and older.

© 2015 by American Society of Clinical Oncology



Prostate Cancer Screening After the 2012 USPSTF Recommendation

men about the purpose of their most recent PSA test (ie, as “part of a routine examination,” “because of a problem,” “other reason,” or “don’t know”). The dependent variable of interest was a PSA test as “part of a routine examination,” which was considered to be a test for screening purposes. Statistical Analyses We incorporated sampling weights into all analyses using the strata and primary sampling units in the database. We determined race/ethnicity, highest education level, marital status, colonoscopy utilization, body mass index, tobacco use, personal cancer history, and self-reported health status. We investigated age-based prostate cancer screening by dividing the cohort into 5-year subgroups. We determined the proportion of each group who had a PSA test in the year before the 2005, 2010, and 2013 surveys. Next, we used an externally validated mortality index designed specifically for the NHIS to calculate each man’s predicted risk of death in the 9 years after the survey.20 The index has only been validated in men age 65 years and older; thus, we limited the analysis investigating screening rates by predicted 9-year mortality risk to this age range. We divided the men into the following two groups: healthier men with a ⱕ 52% predicted risk of 9-year mortality and less healthy men with a more than 52% predicted 9-year mortality. We stratified these men into age groups (65 to 69, 70 to 74, and ⱖ 75 years) and calculated screening rates based on predicted 9-year mortality. We performed univariable analyses using logistic regressions to investigate the association between PSA testing and factors potentially associated with screening in the 2005, 2010, and 2013 surveys. We included men age 65 years and older who visited a physician in the year prior and analyzed self-reported race, highest education level, marital status, alcohol use, tobacco use, colonoscopy utilization, frequency of light or moderately strenuous exercise, body mass index, self-reported personal health status, ability to independently perform activities of daily living, walking ability, chronic anxiety or depression, predicted 9-year mortality risk, nation of origin, diabetes, chronic obstructive pulmonary disease, previously diagnosed cancer (other than prostate cancer), and number of nights hospitalized during the previous year. We constructed two multivariable logistic regression models using variables associated with prostate cancer screening in univariable analyses (P ⬍ .05). Model 1 included all variables significant in univariable analyses. Because many component variables in the mortality index independently predicted screening, we excluded predicted 9-year mortality to reduce the risk of colinearity. Model 2 included predicted 9-year mortality risk but omitted variables used to calculate the 9-year mortality risk variable. Both models included men age 65 and older in the 2005, 2010, and 2013 surveys and excluded men who had not seen a physician in the year prior. Finally, we investigated variables associated with screening changes from 2010 to 2013 by including an interaction-with-age term in logistic regressions (interaction analysis). We used Stata/SE version 13.0 (StataCorp, College Station, TX) and considered a P ⬍ .05 to be statistically significant.

RESULTS

Survey Response Rates and Demographic Characteristics of Respondents (Table 1) Final survey response rates for adults in 2005, 2010, and 2013 were 69%, 61%, and 61%. The final adult survey response incorporated nonresponse at the household and family levels in addition to nonresponse at the individual adult level. The NHIS did not provide demographic data for nonrespondents compared with adults who completed the survey.21 After incorporating survey weights, these results represented approximately 60,813,000 men age 40 years and older in 2005, 66,065,000 in 2010, and 69,660,000 in 2013. In 2005, 2010, and 2013, the rates of all men age 40 years and older who answered prostate cancer screening questions were 88.7%, 90.0%, and 94.7%, respectively. Appendix Table A1 (online only) compares respondents and nonrespondents. The majority of men age 65 years and www.jco.org

Fig 1. Proportion of men, by 5-year age group, who saw a physician in the year prior and received a prostate-specific antigen (PSA) test for screening purposes.

older (97.5%) had insurance coverage from Medicare and/or private insurance. The proportion of men who visited a physician in the year before the 2013 survey was lowest among those age 40 to 49 years (64.4%) and highest among men age 75 years and older (92.0%). Screening Rates by Age Group and Predicted 9-Year Mortality Risk There were no significant differences in screening rates by age group between 2005 and 2010. Rates significantly declined from 2010 to 2013 among all age groups except those age 40 to 49 years (Fig 1). Screening did not significantly differ from 2010 to 2013 among 40- to 49-year-old men (odds ratio [OR], 0.88; P ⫽ .4), with rates of 12.5% (95% CI, 10.2% to 14.7%) and 11.2% (95% CI, 9.2% to 13.2%) in 2010 and 2013, respectively. Notably, men age 60 to 74 years were most heavily screened, with a rate of 51.2% (95% CI, 48.1% to 54.2%) in 2010, declining to 43.6% (95% CI, 41.0% to 46.2%) in 2013 (OR, 0.74; P ⬍ .01). Screening significantly declined for men age 50 to 59 years, from 33.2% (95% CI, 30.1% to 36.3%) in 2010 to 24.8% (95% CI, 22.3% to 27.3%) in 2013 (OR, 0.66; P ⬍ .01), as well as for men age 75 years and older, from 43.9% (95% CI, 39.1% to 48.7%) in 2010 to 37.1% (95% CI, 33.2% to 41.0%) in 2013 (OR, 0.75; P ⫽ .03). After incorporation of sample weights, approximately 1.4 million men age 40 to 49 years, 3.6 million age 50 to 59 years, 6.6 million age 60 to 74 years, and 2.0 million age 75 years and older were screened for prostate cancer in 2013. We performed two sets of sensitivity analyses confirming the trends observed in 2005, 2010, and 2013 (Appendix Figs A1 and A2). The first assumed all nonrespondents did not undergo PSA screening in the year prior, and the second assumed all nonrespondents did (Appendix Figs A1 and A2). Overall, in 2013, men age 65 years and older were screened at a lower rate if they were less healthy and had a higher likelihood (⬎ 52%) of dying in the next 9 years (OR, 0.48; P ⬍ .01; Fig 2). This observation persisted in men age 65 to 69 years (OR, 0.38; P ⬍ .01), 70 to 74 years (OR, 0.44; P ⬍ .01), and 75 years and older (OR, 0.62; P ⫽ .01). Large percentages of men were screened in 2013 despite a high risk (⬎ 52%) of predicted 9-year mortality, as follows: 27.2% (95% CI, © 2015 by American Society of Clinical Oncology


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Fig 2. Prostate cancer screening rates, in 2013, by age group and predicted 9-year mortality among men age 65 years and older who had seen a physician in the year prior.

assistance with activities of daily living, and rated their health more favorably were significantly more likely to be screened (all P ⬍ .05; Table 2). Model 2, which excluded component variables of the 9-year mortality index, demonstrated that men who were white, were more highly educated, were married, had a history of consuming alcohol, received a colonoscopy in the 10 years prior, regularly performed light or moderate activities, and had a lower predicted risk of 9-year mortality were significantly more likely to be screened for prostate cancer (all P ⬍ .05; Table 2). From 2010 to 2013, there were no significant predictors of declines in prostate cancer screening among men age 50 years and older who visited a physician in the year prior. There was a trend toward significance for educationlevelandnationofbirth(UnitedStatesvother) as predictors of declining screening rates from 2010 to 2013 (Table 3). DISCUSSION

16.6% to 37.8%) of men age 65 to 69 years, 32.3% (95% CI, 22.2% to 42.4%) of men age 70 to 74 years, and 32.2% (95% CI, 26.9% to 37.6%) of men age 75 years and older. After incorporation of sample weights, approximately 1.4 million men age 65 years and older with a high risk (⬎ 52%) of predicted 9-year mortality visited a physician and were screened for prostate cancer in 2013. The majority of all PSA tests performed for men younger than age 80 years in 2013 were drawn from healthier men with a low predicted risk of 9-year mortality (ⱕ 52%; Fig 3). The majority of tests (73.3%; 95% CI, 63.7% to 82.9%) ordered for men age 80 years and older were in men unlikely to live another 9 years (⬎ 52% mortality likelihood). Predictors of Screening and Interval Changes in Screening A multivariable model was used to predict screening in men age 65 and older who visited a physician in the year before the 2005, 2010, and 2013 surveys. Model 1, which excluded predicted 9-year mortality, demonstrated that men who were college educated, were married, consumed alcohol, received a colonoscopy in the 10 years before the survey, regularly performed light or moderate activities, did not need

Fig 3. The proportion of all men who saw a physician in the year before the 2013 survey and received a prostate-specific antigen screening test who had ⱕ 52% or more than 52% likelihood of 9-year mortality at time of testing. 4


Prostate cancer screening significantly declined among men age 50 years and older in the United States after the 2012 USPSTF recommendation discouraging PSA-based screening. No specific patientrelated factors predicted declining rates of screening from 2010 to 2013. Despite these declines, in 2013 approximately one third of men age 65 years and older with a high risk (52%) of predicted 9-year mortality were screened—approximately 1.4 million men. Our study is the first to demonstrate national declines in selfreported PSA testing after the 2012 USPSTF recommendation discouraging PSA-based prostate cancer screening. The largest change occurred among men age 50 to 59 years, in whom absolute and relative screening rates decreased by 8% and 25% from 2010 to 2013. Screening decreased among all age groups, similar to other studies examining regional health networks.22,23 This decrease, regardless of age and even in those with lengthy estimated remaining life expectancy, suggests some physicians are adhering to the USPSTF guidelines compared with age-based and life expectancy– based guidelines.3,4,24 Notably, a similar decline was not observed after the 2008 recommendation discouraging prostate cancer screening among men age 75 and older.13,25 Persistently elevated screening rates among men with limited remaining life expectancies are troubling and merit further interventions. These may include increasing awareness of initiatives such as Choosing Wisely recommendations from the American Society of Clinical Oncology and recommendations from the American Geriatrics Society, both of which discourage screening men with limited remaining life expectancies, as well as supporting physician-led quality initiatives such as the Michigan Urological Surgery Improvement Collaborative, which has demonstrated success in other areas of urologic oncology.26-30 Reducing or eliminating reimbursement for screening and subsequent interventions performed for men with limited remaining life expectancies may be considered if physician-led efforts fall short. There are many potential effects of decreased prostate cancer screening after the 2012 USPSTF recommendation. Decreased screening will result in fewer prostate biopsies and fewer men diagnosed with prostate cancer.31-34 Models constructed by Gulati et al35 predicted that a continuation of screening patterns from the year 2000 would result in approximately 710,000 to 1,120,000 overdiagnosed prostate cancers and 280,000 prostate cancer deaths from 2013 to 2025. The predicted number of overdiagnosed cancers would decrease by two thirds in a program limiting testing to men younger than age of 70 JOURNAL OF CLINICAL ONCOLOGY



Table 2. Multivariable Analysis of Predictors for Prostate Cancer Screening Among Men Age 65 and Older in 2005, 2010, or 2013 Who Had Seen a Physician in the Year Prior Model 1,ⴱ Without Mortality Risk Variable Race Non-Hispanic white Non-Hispanic black Hispanic Asian Other Highest education level Some high school High school diploma Some college College degree Marital status Not married Married/living with partner Alcohol use Never drinker Former drinker Current drinker Tobacco use Never smoker Former smoker Current smoker Colonoscopy history Never had colonoscopy Colonoscopy longer than 10 years ago Colonoscopy within last 10 years Activity level Does not perform light/moderate activity Performs light/moderate activities Nationality Born in the United States Not born in the United States BMI Underweight/normal Overweight Obese Self-reported personal health status Excellent/very good Good Fair/poor ADLs Does not need ADL assistance Needs ADL assistance Walking Difficulty walking/cannot walk No difficulty walking 9-year mortality risk Low risk (⬍ 52%) High risk (ⱖ 52%)

OR

95% CI

REF 0.82 0.88 0.75 0.28

Model 2,† With Mortality Risk P

OR

95% CI

P

REF 0.61 to 1.11 0.60 to 1.29 0.42 to 1.32 0.10 to 0.79

.07

REF 0.75 0.86 0.71 0.25

REF 0.56 to 1.01 0.59 to 1.25 0.41 to 1.22 0.09 to 0.70

.01

REF 1.33 1.29 1.62

REF 1.04 to 1.70 0.98 to 1.70 1.21 to 2.15

.01

REF 1.35 1.28 1.66

REF 1.05 to 1.72 0.97 to 1.69 1.25 to 2.21

⬍ .01

REF 1.55

REF 1.30 to 1.85

⬍ .01

REF 1.55

REF 1.31 to 1.85

⬍ .01

REF 1.45 1.60

REF 1.08 to 1.94 1.22 to 2.09

⬍ .01

REF 1.49 1.68

REF 1.12 to 1.97 1.30 to 2.17

⬍ .01

REF 1.08 0.94

REF 0.90 to 1.31 0.69 to 1.27

.5

REF 1.02 1.78

REF 0.70 to 1.48 1.47 to 2.15

⬍ .01

REF 1.10 1.80

REF 0.76 to 1.59 1.49 to 2.17

⬍ .01

REF 1.23

REF 1.03 to 1.47

.02

REF 1.25

REF 1.05 to 1.50

.01

REF 0.89

REF 0.63 to 1.26

.5

REF 0.88

REF 0.63 to 1.25

.5

REF 1.20 1.21

REF 0.98 to 1.46 0.97 to 1.50

.1

REF 0.84 0.70

REF 0.68 to 1.02 0.54 to 0.90

.02

REF 0.82

REF 0.68 to 0.98

.03

REF 0.95

REF 0.89 to 1.02

.2

REF 0.60

REF 0.49 to 0.72

⬍ .01

Abbreviations: ADL, activities of daily living; BMI, body mass index; OR, odds ratio; REF, reference. ⴱ Model 1 omits the predicted 9-year mortality variable to reduce colinearity. †Model 2 omits the component variables used to calculate the 9-year mortality variable.

years, but prostate cancer deaths would increase by 5% to 8%. Predicted prostate cancer deaths would increase by 13% to 20% in a program completely discontinuing screening. These models did not account for contemporary guideline nonadherence in the form of persistent screening of men of advanced age and/or limited remaining www.jco.org

life expectancy, an important distinction because approximately 80% of men age 75 and older diagnosed with prostate cancer pursue active treatment.12,13,35,36 Patients at low risk for prostate cancer may be monitored with extended screening intervals, an approach reinforced by data from the © 2015 by American Society of Clinical Oncology


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Table 3. Changes in Prostate Cancer Screening Rates From 2010 to 2013 Among Men Age 50 Years and Older According to Demographic, Behavioral, and Disease Factors and Predicted Mortality Risk Variable

Odds Ratioⴱ

Race Non-Hispanic white 0.72 Non-Hispanic black 0.89 Hispanic 0.84 Asian 0.54 Other 0.44 Highest education level Some high school 0.87 High school diploma 0.78 Some college 0.75 College degree 0.58 Marital status Not married 0.74 Married/Living with partner 0.67 Alcohol use Never drinker 0.69 Former drinker 0.64 Current drinker 0.75 Tobacco use Never smoker 0.77 Former smoker 0.72 Current smoker 0.60 Colonoscopy history Never had colonoscopy 0.80 Colonoscopy longer than 10 years ago 0.55 Colonoscopy within last 10 years 0.71 Activity level Does not perform light/moderate activity 0.74 Performs light/moderate activities 0.69 Nationality Born in the United States 0.70 Not born in the United States 0.91 COPD No history of COPD 0.72 History of COPD 0.66 Diabetes No history of diabetes 0.70 History of diabetes 0.79 Personal history of cancer No personal history of cancer 0.71 Personal history of cancer 0.81 Hospitalizations in past year No hospitalization 0.74 One night in hospital in past year 0.58 Multiple nights in hospital in past year 0.64 BMI Underweight/normal 0.72 Overweight 0.77 Obese 0.67 Self-reported personal health status Excellent/very good 0.68 Good 0.79 Fair/poor 0.75 ADLs Does not need ADL assistance 0.72 Needs ADL assistance 0.66 (continued in next column)

6


95% CI†

P

0.63 to 0.81 0.66 to 1.20 0.57 to 1.24 0.30 to 1.0 0.17 to 1.14

.3

0.64 to 1.18 0.62 to 0.98 0.60 to 0.93 0.48 to 0.70

.1

0.65 to 0.85 0.56 to 0.80

.4

0.51 to 0.95 0.51 to 0.80 0.66 to 0.86

.4

0.66 to 0.89 0.61 to 0.86 0.44 to 0.81

.4

0.65 to 0.98 0.31 to 0.97 0.58 to 0.87

.4

0.62 to 0.87 0.60 to 0.80

.6

0.63 to 0.79 0.66 to 1.25

.1

0.65 to 0.81 0.45 to 0.97

.6

0.62 to 0.80 0.63 to 1.0

.4

0.64 to 0.80 0.55 to 1.19

.6

0.66 to 0.84 0.41 to 0.82 0.37 to 1.13

.4

0.57 to 0.91 0.65 to 0.90 0.55 to 0.81

.6

0.58 to 0.79 0.65 to 0.96 0.60 to 0.95

.4

0.65 to 0.81 0.41 to 1.07

.7

Table 3. Changes in Prostate Cancer Screening Rates From 2010 to 2013 Among Men Age 50 Years and Older According to Demographic, Behavioral, and Disease Factors and Predicted Mortality Risk (continued) Variable Walking Difficulty walking/cannot walk No difficulty walking Anxiety No history of anxiety or depression Anxiety and/or depression 9-year mortality risk‡ Low risk (⬍ 52%) High risk (ⱖ 52%)

Odds Ratioⴱ

95% CI†

P

0.70 0.77

0.61 to 0.80 0.63 to 0.95

.5

0.73 0.55

0.65 to 0.81 0.26 to 1.17

.5

0.85 0.70

0.70 to 1.04 0.52 to 0.93

.3

Abbreviations: ADL, activities of daily living; BMI, body mass index; COPD, chronic obstructive pulmonary disease; OR, odds ratio. ⴱ OR ⬍ 1 indicates a decline and OR ⬎ 1 indicates an increase in prostatespecific antigen screening rate. †P value for interaction with year. ‡Only men age 65 years and older were assessed for 9-year mortality risk because the index is only validated for men in this age group.

European Randomized Study of Screening for Prostate Cancer, the newest American Urological Association recommendation, and other previously published studies.2,24,37,38 Modeling studies from the Rotterdam component of the European Randomized Study of Screening for Prostate Cancer demonstrated that annual screening of men age 55 to 67 years results in an overdiagnosis rate of 50%.39 Heijnsdijk et al40 demonstrated that greatest cost-effectiveness was achieved with a screening program offered to patients between age 55 and 60 years with 1- to 2-year intervals. Gulati et al37 showed that men with PSA values less than the median age group–matched levels may be screened up to every 5 years without dramatically impacting patient-centered outcomes. The approach of Gulati et al37 would reduce overdiagnoses by approximately 27% and false-positive results by 50%, yet would still save 83% of lives compared with an annual screening interval approach. A prospective study by Aus et al38 similarly demonstrated that men age 50 to 66 years with low baseline serum PSA levels could be safely screened every 3 years with minimal effects on prostate cancer–specific mortality. The contemporary objective of screening is the detection of highvolume or high-grade cancers that are likely to become clinically evident. A physician caring for a patient with an elevated PSA level should interpret the value relative to age-specific controls and not reflexively proceed to biopsy, because up to 55% of elevated PSA levels will normalize within the course of 1 year. The NHIS does not provide data regarding the percentage of men with elevated PSA levels who proceeded to have a prostate biopsy. The probability of highrisk cancer should be estimated using existing validated risk calculators.41-45 Multiple novel biomarkers have also recently become commercially available to improve on PSA alone in predicting the likelihood of a man harboring a high-grade cancer. Tests such as the prostate CA 3, kallikrein panel, and Prostate Health Index have superior operating characteristics compared with PSA alone.46-48 The adoption and integration of these tests, along with downstream effects, require further study. Limitations of the NHIS database include its interview-based reporting component. A meta-analysis investigating agreement between self-reported cancer screening and medical records, however, JOURNAL OF CLINICAL ONCOLOGY



indicated a tendency toward under-reporting of prostate cancer screening.49 Similarly, informative details about ordering provider (primary care physician or specialist) or practice structure (private, academic, and so on) were not available. Data regarding survey nonrespondents were not provided by the NHIS, which limited the investigation of potential selection biases. The overall survey response rate for prostate cancer screening questions, however, was high (91.2%), and sensitivity analyses (Appendix Figs A1 and A2, Appendix Table A1) demonstrated preserved prostate cancer screening trends after the 2012 USPSTF guideline. We limited this analysis to men who visited a physician in the year before the survey, which only captures screening behavior among individuals who interfaced with the health care system. This contrasts with an analysis performed in 2011 in which we analyzed screening among all men regardless of their interaction with the health care system.11 The USPSTF recommendation was finalized in May 2012, which allowed for a relatively short amount of time for dissemination of the guidelines into practice. Nevertheless, the guideline was covered widely in every major media outlet, was likely known to an overwhelming majority of primary care physicians and urologists, and has clearly impacted clinical practice. In conclusion, this is the first analysis demonstrating a nationwide decline in national prostate cancer screening rates among men REFERENCES 1. Andriole GL, Crawford ED, Grubb RL 3rd, et al: Mortality results from a randomized prostatecancer screening trial. N Engl J Med 360:1310-1319, 2009 2. Schröder FH, Hugosson J, Roobol MJ, et al: Screening and prostate-cancer mortality in a randomized European study. N Engl J Med 360:13201328, 2009 3. Moyer VA, US Preventive Services Task Force: Screening for prostate cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med 157:120-134, 2012 4. Wolf AM, Wender RC, Etzioni RB, et al: American Cancer Society guideline for the early detection of prostate cancer: Update 2010. CA Cancer J Clin 60:70-98, 2010 5. Greene KL, Albertsen PC, Babaian RJ, et al: Prostate specific antigen best practice statement: 2009 update. J Urol 182:2232-2241, 2009 6. Qaseem A, Barry MJ, Denberg TD, et al: Screening for prostate cancer: A guidance statement from the Clinical Guidelines Committee of the American College of Physicians. Ann Intern Med 158:761-769, 2013 7. American Academy of Family Physicians: Clinical Preventive Service Recommendation: Prostate Cancer. http://www.aafp.org/patient-care/clinicalrecommendations/all/prostate-cancer.html 8. Lim LS, Sherin K, ACPM Prevention Practice Committee: Screening for prostate cancer in U.S. men ACPM position statement on preventive practice. Am J Prev Med 34:164-170, 2008 9. Kawachi MH, Bahnson RR, Barry M, et al: NCCN clinical practice guidelines in oncology: Prostate cancer early detection. J Natl Compr Canc Netw 8:240-262, 2010 10. Tasian GE, Cooperberg MR, Cowan JE, et al: Prostate specific antigen screening for prostate cancer: Knowledge of, attitudes towards, and utilization among primary care physicians. Urol Oncol 30:155160, 2012 www.jco.org

age 50 years and older after the 2012 USPSTF guideline discouraging PSA testing for the early detection of prostate cancer. Encouragingly, an increased probability of 9-year mortality was associated with decreased screening rates from 2010 to 2013. Despite these trends, roughly a third of men older than age 65 years with a high probability (⬎ 52%) of death within the next 9 years were screened for prostate cancer, exposing these approximately 1.4 million men to a high risk of overdiagnosis and overtreatment. AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST Disclosures provided by the authors are available with this article at www.jco.org.

AUTHOR CONTRIBUTIONS Conception and design: All authors Collection and assembly of data: Michael W. Drazer, Dezheng Huo Data analysis and interpretation: All authors Manuscript writing: All authors Final approval of manuscript: All authors

11. Drazer MW, Huo D, Schonberg MA, et al: Population-based patterns and predictors of prostatespecific antigen screening among older men in the United States. J Clin Oncol 29:1736-1743, 2011 12. Drazer MW, Prasad SM, Huo D, et al: National trends in prostate cancer screening among older American men with limited 9-year life expectancies: Evidence of an increased need for shared decision making. Cancer 120:1491-1498, 2014 13. Prasad SM, Drazer MW, Huo D, et al: 2008 US Preventive Services Task Force recommendations and prostate cancer screening rates. JAMA 307: 1692-1694, 2012 14. Harris G: U.S. panel says no to prostate screening for healthy men. The New York Times, 2011. http://www.nytimes.com/2011/10/07/health/ 07prostate.html?_r⫽0 15. Kaiser Health News, Kaiser Family Foundation: New England Journal of Medicine weighs in with views on PSA testing. KHN Morning Briefing. 2011. http:// kaiserhealthnews.org/morning-breakout/thur-opinionnejm-on-psa-testing/ 16. Bankhead C: Prostate test recommendation draws mixed reviews. MedPage Today, 2011. http:// www.medpagetoday.com/HematologyOncology_/ ProstateCancer/29015 17. Selyukh A: Health panel takes heat on cancer screening advice. Health, Reuters, 2011. http:// www.reuters.com/article/2011/12/18/us-healthtaskforce-idUSTRE7BH0C620111218 18. Kane J: PSA testing controversy reignites “overscreening” debate. PBS Newshour, 2011. http:// www.pbs.org/newshour/rundown/psa-testingcontroversy-reignites-over-screening-debate/ 19. Prabhu V, Lee T, Loeb S, et al: Twitter response to the United States Preventive Services Task Force recommendations against screening with prostate specific antigen. BJU Int [epub ahead of print on March 25, 2014] 20. Schonberg MA, Davis RB, McCarthy EP, et al: External validation of an index to predict up to 9-year mortality of community-dwelling adults aged 65 and older. J Am Geriatr Soc 59:1444-1451, 2011

21. National Center for Health Statistics: National Health Interview Survey. Public-use data file and documentation. http://www.cdc.gov/nchs/nhis/quest_ data_related_1997_forward.htm 22. Cohn JA, Wang CE, Lakeman JC, et al: Primary care physician PSA screening practices before and after the final U.S. Preventive Services Task Force recommendation. Urol Oncol 32:41.e2341.e30, 2014 23. Aslani A, Minnillo BJ, Johnson B, et al: The impact of recent screening recommendations on prostate cancer screening in a large health care system. J Urol 191:1737-1742, 2014 24. Carter HB, Albertsen PC, Barry MJ, et al: Early detection of prostate cancer: AUA Guideline. J Urol 190:419-426, 2013 25. US Preventive Services Task Force: Screening for prostate cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med 149:185-191, 2008 26. American Society of Clinical Oncology: Choosing Wisely, American Society of Clinical Oncology: 10 things physicians and patients should question. http://www.choosingwisely.org 27. American Geriatrics Society: Choosing Wisely, American Geriatrics Society: 10 things physicians and patients should question. http://www .choosingwisely.org 28. Riedinger CB, Womble PR, Linsell SM, et al: Variation in prostate cancer detection rates in a statewide quality improvement collaborative. J Urol 192:373-378, 2014 29. Womble PR, Montie JE, Ye Z, et al: Contemporary use of initial active surveillance among men in Michigan with low-risk prostate cancer. Eur Urol 67:44-50, 2015 30. Filson CP, Boer B, Curry J, et al: Improvement in clinical TNM staging documentation within a prostate cancer quality improvement collaborative. Urology 83:781-786, 2014 31. Wade J, Rosario DJ, Macefield RC, et al: Psychological impact of prostate biopsy: Physical symptoms, anxiety, and depression. J Clin Oncol 31:4235-4241, 2013



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32. Loeb S, Carter HB, Berndt SI, et al: Complications after prostate biopsy: Data from SEERMedicare. J Urol 186:1830-1834, 2011 33. Nam RK, Saskin R, Lee Y, et al: Increasing hospital admission rates for urological complications after transrectal ultrasound guided prostate biopsy. J Urol 183:963-968, 2010 34. Loeb S, Vellekoop A, Ahmed HU, et al: Systematic review of complications of prostate biopsy. Eur Urol 64:876-892, 2013 35. Gulati R, Tsodikov A, Etzioni R, et al: Expected population impacts of discontinued prostate-specific antigen screening. Cancer 120:3519-3526, 2014 36. Cooperberg MR, Broering JM, Carroll PR: Time trends and local variation in primary treatment of localized prostate cancer. J Clin Oncol 28:1117-1123, 2010 37. Gulati R, Gore JL, Etzioni R: Comparative effectiveness of alternative prostate-specific antigen– based prostate cancer screening strategies: Model estimates of potential benefits and harms. Ann Intern Med 158:145-153, 2013 38. Aus G, Damber JE, Khatami A, et al: Individualized screening interval for prostate cancer based on prostate-specific antigen level: Results of a pro-

spective, randomized, population-based study. Arch Intern Med 165:1857-1861, 2005 39. Draisma G, Boer R, Otto SJ, et al: Lead times and overdetection due to prostate-specific antigen screening: Estimates from the European Randomized Study of Screening for Prostate Cancer. J Natl Cancer Inst 95:868-878, 2003 40. Heijnsdijk EA, de Carvalho TM, Auvinen A, et al: Cost-effectiveness of prostate cancer screening: A simulation study based on ERSPC data. J Natl Cancer Inst 107:366, 2015 41. Oesterling JE, Jacobsen SJ, Chute CG, et al: Serum prostate-specific antigen in a communitybased population of healthy men: Establishment of age-specific reference ranges. JAMA 270:860-864, 1993 42. Eastham JA, Riedel E, Scardino PT, et al: Variation of serum prostate-specific antigen levels: An evaluation of year-to-year fluctuations. JAMA 289:2695-2700, 2003 43. UT Health Science Center: Individualized risk assessment of prostate cancer. http://deb.uthscsa.edu/ URORiskCalc/Pages/uroriskcalc.jsp 44. Thompson IM, Ankerst DP, Chi C, et al: Assessing prostate cancer risk: Results from the Pros-

tate Cancer Prevention Trial. J Natl Cancer Inst 98:529-534, 2006 45. Parekh DJ, Ankerst DP, Higgins BA, et al: External validation of the Prostate Cancer Prevention Trial risk calculator in a screened population. Urology 68:1152-1155, 2006 46. Vedder MM, de Bekker-Grob EW, Lilja HG, et al: The added value of percentage of free to total prostate-specific antigen, PCA3, and a kallikrein panel to the ERSPC risk calculator for prostate cancer in prescreened men. Eur Urol 66:1109-1115, 2014 47. Nordström T, Vickers A, Assel M, et al: Comparison between the four-kallikrein panel and Prostate Health Index for predicting prostate cancer. Eur Urol [epub ahead of print on August 20, 2014] 48. Wei JT, Feng Z, Partin AW, et al: Can urinary PCA3 supplement PSA in the early detection of prostate cancer? J Clin Oncol 32:4066-4072, 2014 49. Rauscher GH, Johnson TP, Cho YI, et al: Accuracy of self-reported cancer-screening histories: A meta-analysis. Cancer Epidemiol Biomarkers Prev 17:748-757, 2008

■ ■ ■

GLOSSARY TERMS

biomarker: a functional biochemical or molecular indicator of a biologic or disease process that has predictive, diagnostic, and/or prognostic utility. life expectancy: the average number of years that an individual would live if he or she were to experience throughout life the age-specific mortality rates prevailing in a given year.

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prostate-specific antigen (PSA): a protein produced by cells of the prostate gland. The blood level of prostate-specific antigen (PSA) is used as a tumor marker for men who may be suspected of having prostate cancer. Most physicians consider 0 to 4.0 ng/mL to be the normal range. Levels of 4 to 10 and 10 to 20 ng/mL are considered slightly and moderately elevated, respectively. PSA levels have to be complemented with other tests to make a firm diagnosis of prostate cancer.




AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

National Prostate Cancer Screening Rates After the 2012 US Preventive Services Task Force Recommendation Discouraging Prostate-Specific Antigen–Based Screening The following represents disclosure information provided by authors of this manuscript. All relationships are considered compensated. Relationships are self-held unless noted. I ⫽ Immediate Family Member, Inst ⫽ My Institution. Relationships may not relate to the subject matter of this manuscript. For more information about ASCO’s conflict of interest policy, please refer to www.asco.org/rwc or jco.ascopubs.org/site/ifc. Michael W. Drazer No relationship to disclose Dezheng Huo No relationship to disclose

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Scott E. Eggener Consulting or Advisory Role: Myriad Genetics, Medivation, Janssen Pharmaceuticals, Genomic Health, OPKO Diagnostics, MDxHealth Speakers’ Bureau: Myriad Genetics, Janssen Pharmaceuticals Research Funding: Myriad Genetics (Inst)




Appendix

Table A1. Survey Respondents (answered questions about prostate cancer screening) Versus Nonrespondents No. (%) Characteristic Race/ethnicity Non-Hispanic white Non-Hispanic black Hispanic Asian Other Highest education level Some high school High school diploma Some college College degree Marital status Not married Married/living with partner Colonoscopy history Never had colonoscopy Colonoscopy longer than 10 years ago Colonoscopy within last 10 years Body mass index Underweight/normal Overweight Obese Tobacco use Never smoker Former smoker Current smoker Personal cancer history No personal history of cancer Personal history of cancer Self-reported personal health status Excellent/very good Good Fair/poor Age, years 40-49 50-59 60-74 75⫹ Survey year 2005 2010 2013 Visited physician in year prior Visited a physician Did not visit a physician 9-year predicted mortality riskⴱ Low risk High risk

Respondents (n ⫽ 22,490)

Nonrespondents (n ⫽ 2,168)

P ⬍ .01

14,917 (74.0) 2,986 (9.4) 3,196 (11.2) 1,017 (4.1) 374 (1.3)

1,420 (74.3) 350 (10.5) 257 (9.2) 116 (4.6) 25 (1.4)

3,994 (15.0) 6,126 (27.4) 5,798 (26.1) 6,454 (27.5)

424 (16.9) 634 (30.3) 510 (25.4) 539 (27.5)

8,750 (25.6) 13,690 (74.4)

991 (31.3) 1,138 (68.7)

13,216 (73.2) 580 (3.2) 4,215 (23.6)

399 (65.9) 19 (2.1) 197 (32.0)

5,799 (24.5) 9,936 (44.9) 6,558 (30.6)

554 (28.8) 803 (42.5) 496 (28.8)

10,304 (46.8) 7,420 (33.1) 4,734 (20.1)

898 (46.1) 686 (34.2) 428 (19.7)

21,401 (95.2) 1,077 (4.8)

2,017 (93.7) 131 (6.3)

11,742 (55.0) 6,651 (28.9) 4,087 (16.1)

1,002 (49.9) 649 (28.1) 514 (22.0)

7,048 (34.0) 6,616 (30.4) 6,405 (26.6) 2,421 (9.1)

602 (30.0) 619 (30.1) 604 (26.5) 343 (13.4)

7,278 (30.4) 6,301 (32.8) 8,911 (36.8)

926 (38.1) 742 (41.3) 500 (20.6)

16,520 (75.0) 5,954 (25.1)

1,401 (77.5) 412 (22.5)

4,185 (69.4) 1,965 (30.6)

401 (58.4) 311 (41.6)

.1

.2

.03

.6

.5

.6

⬍ .01

⬍ .01

⬍ .01

⬍ .01

⬍ .01†

ⴱ Only for men age 65 and older. †Univariable analysis only.




Prostate Cancer Screening Rates (%)


60 50

2005 2010 2013

40 30 20 10 0 65-69

70-74

75-79

80-84

Age Group (years) Fig A1. Screening rates by year. Sensitivity analysis assuming all nonrespondents did not have a prostate cancer screen in the year before the survey.

Fig A2. Screening rates by year. Sensitivity analysis assuming all nonrespondents had a prostate cancer screen in the year before the survey.

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