Oncology: Prostate/Testis/Penis/Urethra

Decline in Prostate Cancer Screening by Primary Care

Physicians: An Analysis of Trends in the Use of Digital
Rectal Examination and Prostate Specific Antigen Testing
Jonathan Shoag,* Joshua A. Halpern, Daniel J. Lee, Sameer Mittal,
Karla V. Ballman, Christopher E. Barbieri and Jim C. Hu
From the Department of Urology, New York Presbyterian Hospital and Department of Biostatistics and Epidemiology (KVB),
Weill Cornell Medical College, New York, New York

Purpose: Prostate cancer screening by digital rectal examination and prostate

Abbreviations
specific antigen testing has been routine clinical practice in the United States for
and Acronyms
the last 25 years. Recent studies have shown a national decline in prostate
specific antigen testing following the USPSTF (United States Preventive DRE digital rectal examination
Services Task Force) recommendation against routine prostate specific antigen PCP primary care physician
screening. However, to our knowledge the effect of this recommendation on PLCO Prostate, Lung, Colorectal
digital rectal examination utilization remains unknown. and Ovarian
Materials and Methods: We used NAMCS (National Ambulatory Medical Care PSA prostate specific antigen
Survey) to characterize trends in the rate of digital rectal examination and
prostate specific antigen testing by primary care physicians in men older than Accepted for publication March 19, 2016.
No direct or indirect commercial incentive
40 years presenting for preventive care. From 2005 to 2012 NAMCS contained associated with publishing this article.
3,368 such visits (unweighted) for the study of digital rectal examination trends The corresponding author certifies that, when
and 4,035 unweighted visits from 2002 to 2012 for the study of prostate specific applicable, a statement(s) has been included in
the manuscript documenting institutional review
antigen trends. board, ethics committee or ethical review board
Results: Following the USPSTF recommendation the proportion of visits where study approval; principles of Helsinki Declaration
were followed in lieu of formal ethics committee
digital rectal examination was performed decreased from 16.0% (95% CI
approval; institutional animal care and use
13.1e19.5) to 5.8% (95% CI 4.0e8.3, p <0.001). Similarly, the proportion of visits committee approval; all human subjects provided
where prostate specific antigen testing was performed decreased from 27.3% written informed consent with guarantees of
(95% CI 24.5e30.3) to 16.7% (95% CI 12.9e21.2, p <0.001). This represents a confidentiality; IRB approved protocol number;
animal approved project number.
relative 64% decrease in digital rectal examination and a 39% decrease in * Correspondence: Weill Cornell Medical
prostate specific antigen testing. Among men 55 to 69 years old the number of College, 525 East 70th St., Starr 900, New York,
New York 10065 (telephone: 212-746-5455;
visits where digital rectal examination and prostate specific antigen testing were
e-mail: jes9171@nyp.org).
performed decreased 65% and 39%, respectively (p <0.001). Equal study contribution.
Conclusions: Utilization of digital rectal examination and prostate specific
antigen has declined significantly following the release of the USPSTF recom-
mendation against prostate specific antigen screening. This suggests that
prostate cancer screening is rapidly disappearing from primary care practice.

Key Words: prostatic neoplasms, mass screening, prostate specific antigen,

digital rectal examination, practice guideline

DIGITAL rectal examination and PSA screening protocols in the early 1980s
testing have been a part of routine relied only on DRE, the absence
preventive care in the United States of evidence supporting a definitive
for the last 25 years. While initial mortality benefit to DRE alone led to

0022-5347/16/1964-1047/0 http://dx.doi.org/10.1016/j.juro.2016.03.171
THE JOURNAL OF UROLOGY
2016 by AMERICAN UROLOGICAL ASSOCIATION EDUCATION AND RESEARCH, INC.
Vol. 196, 1047-1052, October 2016
Printed in U.S.A.
www.jurology.com j 1047
1048 DECLINE IN PROSTATE CANCER SCREENING BY PRIMARY CARE PHYSICIANS
the addition of PSA as a second component to
prostate cancer screening in the early 1990s.1e11
Two large-scale, randomized, controlled trials of
prostate cancer screening were subsequently initi-
ated in part to address concerns regarding over
diagnosis and overtreatment of prostate cancer with
the use of PSA. In October 2011 following the
discordant results of these trials the USPSTF issued
a recommendation against routine PSA screening.12
However, this recommendation failed to explicitly
address the role and efficacy of DRE.
The USPSTF recommendation dramatically
reshaped the landscape of prostate cancer screening
and treatment in the United States. Multiple
studies have demonstrated a national decline in
PSA testing, reduction in prostate biopsies and even
stage migration in diagnosed prostate cancers
following the USPSTF recommendation.12e16
However, the growing literature has largely
omitted DRE, which has been a mainstay of pros-
tate cancer screening for decades that predates
PSA screening. To our knowledge the impact of the
USPSTF recommendation on use of DRE remains
unstudied.
Given expert concern that decreased prostate
cancer screening may lead to adverse oncologic
outcomes, it is critical that policy makers under-
stand the downstream effects of the USPSTF
recommendation not only on PSA but also on DRE
use.16 In this study we assessed temporal trends in
DRE and PSA for prostate cancer screening by
PCPs following the USPSTF recommendation.
METHODS
NAMCS is performed annually by the NCHS (National
Center for Health Statistics) of the CDC (Centers for
Disease Control and Prevention). NAMCS is based on a
sample of patient visits to nonfederal, office based physi-
cians. NAMCS estimates are derived by a multistage
estimation procedure with each visit weighted to extrap-
olate national estimates. As such, each record on the data
files represents between 1 and thousands of actual visits
depending on the survey. The sampling weight is a
product of the reciprocal of the sampling proportions at
each stage in the multistage sampling process, including a
post-ratio adjustment factor. National estimates are
generated from samples so that each estimate is sur-
rounded by a margin of error.17
Physician use of DRE and PSA testing for prostate
cancer screening is captured by NAMCS. We utilized
NAMCS data from 2002 to 2012 for analysis of trends in
PSA testing and NAMCS data from 2005 to 2012 for
analysis of trends in DRE since DRE is coded uniquely for
these years. NAMCS previously included community
health centers, which were excluded in 2012 and, there-
fore, analysis was restricted to noncommunity health
center visits.17 The NCHS institutional review board
approved the protocols for NAMCS/NHAMCS (National
Hospital Ambulatory Medical Care Survey), including a
waiver of the requirement for patient informed consent.
NAMCS recommendations suggest use of a minimum
of 30 unweighted observations to make reliable estimates,
thus, precluding detailed characterization of the popula-
tion that underwent DRE or PSA testing due to the
limited number of examinations performed after release
of the USPSTF recommendation. Of 1,279 unweighted
observations after the recommendation only 68 showed
that a rectal examination was performed and 180 showed
a PSA test. Descriptive variables for each patient
encounter included patient age, primary reason for pa-
tient visit, whether the physician was the patient PCP,
and whether PSA testing and/or DRE was performed.
Statistical analysis was performed in accordance with
NCHS recommendations, accounting for the complex
survey design using STATA/SE, version 13.1.18 The
Pearson chi-square test was used to compare aggregate
rates of screening before and after the 2011 USPSTF
recommendation. Sensitivity analysis restricted to 2010
and 2012 was performed. Trends were illustrated using a
lowess curve for graphical purposes.
RESULTS
Between 2005 and October 2011, when the USPSTF
first recommended against routine PSA screening,
men 40 years old or older seeing their primary care
physician for preventive care comprised 110 million
weighted (2,089 unweighted) visits for the study of
trends in DRE. To study trends in PSA testing
before the USPSTF recommendation from 2002 to
October 2011 men 40 years old or older seeing their
PCP for preventive care comprised 146 million
(2,756 unweighted) visits. Following the USPSTF
recommendation from October 2011 to December
2012 there were 22 million (1,279 unweighted) visits
eligible for study.
Figure 1 shows the annual proportion of visits
where prostate cancer screening was performed.
After the USPSTF recommendation the proportion
of visits where DRE was performed decreased from
16.0% (95% CI 13.1e19.5) to 5.8% (95% CI 4.0e8.3,
p <0.001). Similarly, the proportion of visits where
PSA testing was performed decreased from 27.3%
(95% CI 24.5e30.3) to 16.7% (95% CI 12.9e21.2,
p <0.001). This translates to a relative 64% decrease
in DRE and a relative 39% decrease in PSA testing
after release of the USPSTF recommendation.
Sensitivity analysis comparing only 2010 to 2012
demonstrated a significant decrease during these
survey years in PSA testing and DRE (p 0.003
and <0.001, respectively).
We performed subset analysis in men 55 to 69 years
old, for whom PSA guidelines are discrepant.12,19,20
The rate of digital rectal examination in this group
decreased from 18.2% (95% CI 13.9e23.6) to 6.3%
(95% CI 4.0e9.8, p <0.001). The rate of PSA testing
among these men decreased from 32.6% (95% CI
 DECLINE IN PROSTATE CANCER SCREENING BY PRIMARY CARE PHYSICIANS 1049

Figure 1. Mean and 95% CI of proportion of primary care visits for preventive care in men older than 40 years in whom PCP prostate
cancer screening was performed before and after USPSTF recommendation release. Blue dotted line indicates mean before release.
Green dotted line indicates mean after release. A, DRE. B, PSA test.

28.2e37.4) to 19.9% (95% CI 15.3e25.5, p <0.001)
following the recommendation. Figure 2 shows the
rate of PSA testing by age. We were unable to char-
acterize the use of DRE by age due to the limited
number of examinations that were performed after
release of the USPSTF recommendation.
DISCUSSION
The USPSTF recommendation against PSA
screening has dramatically altered prostate cancer
care in the United States through subsequent
declines in PSA testing, prostate biopsies and
prostate cancer diagnoses.13e15,21,22 While the
USPSTF recommendation did not prescribe the role
of DRE in prostate cancer screening, we found a
substantial reduction in DRE following the recom-
mendation, which was of greater relative magnitude
than the reduction in PSA testing. Currently, the
AUA (American Urological Association) recom-
mends DRE only as an adjunct to PSA screening.20
Our findings demonstrate that many PCPs have
discarded both components of prostate cancer
screening entirely and a reassessment of prostate
cancer screening guidelines may be appropriate to
clarify the role of DRE in routine clinical practice.
In the prePSA era studies of DRE suggested that
it was a cost-effective prostate cancer screening test
with 69% sensitivity and 89% specificity.5e7 While
subsequent studies have questioned the mortality
benefit of DRE screening programs, there is a
dearth of literature examining the role of DRE and
the prognostic implications of a suspicious DRE
after the rapid adoption of PSA screening and
resultant stage migration.9,16,23 Nonetheless, the
USPSTF recommendation has resulted in large-
scale abandonment of DRE in advance of any
conclusive evidence.
1050 DECLINE IN PROSTATE CANCER SCREENING BY PRIMARY CARE PHYSICIANS

absence of screening a potential shift toward diag-

Figure 2. Smoothed curve demonstrates PSA screening by age
in men presenting to PCP for preventive care.
The decrease in both screening tests in men 55 to
69 years old is of particular concern as guidelines
are discrepant in this age group.12,19,20 This sug-
gests that the response of primary care physicians
to current conflicting recommendations has not
been to screen more selectively in only those
who may benefit. Rather, the data suggest that
screening has been broadly abandoned altogether. A
similar trend of widespread decreases in screening
in all age groups has also been identified in other
studies examining declining screening rates.13e15
The rapid decline in both elements of prostate
cancer screening is concerning. Based on United
States epidemiological data the use of DRE and PSA
coincided with prostate cancer increasingly being
detected at an earlier, treatable stage.16,24 In the
nosing more advanced and metastatic cancer is
likely.16,24 For instance, in the prePSA era the
likelihood of lymph node metastases at radical
prostatectomy was about 40% compared to less than
10% prior to the USPSTF recommendation.25
This study must be evaluated in the context of
certain limitations. 1) NAMCS uses a multistage
probability design to estimate national practice
patterns from relatively small patient samples,
which may inaccurately estimate PSA and DRE
utilization trends. 2) Data were limited in 2012 by a
lower than normal response rate as well as a shift to
electronic responses in that survey year. 3) NAMCS
also does not capture information about shared
decision making between patient and physician,
which may contribute to DRE and PSA utilization.
4) Given the short interval since the USPSTF
recommendation, it is not possible to determine the
sustainability of the decrease in prostate cancer
screening. Longer followup studies are required.
CONCLUSIONS
Utilization of DRE and PSA for prostate cancer
screening has declined significantly following the
USPSTF recommendation against PSA screening.
Given the absence of data on the role of DRE in
prostate cancer screening in the post-PSA era, this
rapid decrease in the use of DRE should raise
additional concerns about the future of prostate
cancer care in the United States.

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16. Penson DF: The pendulum of prostate cancer
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EDITORIAL COMMENT

Engaging in shared decision making about the pros
and cons of PSA screening might be challenging
for PCPs who work under time constraint. The
imperative from USPSTF in 2011 to not use PSA
screening for prostate cancer (reference 12 in
article), thus, allowed PCPs to dispense with the
complexities and abandon screening. Several
studies now show decreases in PSA testing after the
recommendation. The current study confirms this
and also shows a decrease in the utilization of DRE
(reference 12 in article).1 These observations call
into question whether PCPs should wait for urinary
retention or spinal cord compression before thinking
about checking a prostate.
Abandoning screening is not in the best interest
of our patients. We do not need a blanket rejection
against an effective means of preventing metastatic
disease and prostate cancer death. We need to
screen, biopsy and treat smarter to keep the benefit
and avoid the harm. Stop screening older men, stop
performing biopsies unless we have compelling
reasons and increase the adoption of active sur-
veillance for low risk disease.1
Sigrid Carlsson*
Departments of Surgery and Epidemiology and Biostatistics
Memorial Sloan Kettering Cancer Center
New York, New York
and
Institute of Clinical Sciences
Department of Urology
Sahlgrenska Academy at Gothenburg University
Gothenburg, Sweden
*Supported by National Cancer Institute Cancer Center Support Grant P30 CA008748
(Memorial Sloan Kettering Cancer Center) and an AFA Insurance postdoctoral research grant.

REFERENCE
1. Vickers AJ, Eastham JA, Scardino PT et al: The Memorial Sloan Kettering Cancer Center recommendations for prostate cancer screening. Urology 2016; 91: 12.

REPLY BY AUTHORS

We agree that the abandonment of prostate cancer
screening in the United States is problematic and a
rapid course correction is needed. The decline in
screening is particularly disconcerting in light of
our recent analysis of testing rates in the PLCO
Cancer Screening Trial. The PLCO trial showed no
difference in prostate cancer specific mortality be-
tween men randomized to annual prostate cancer
screening or usual care1 and it represents the only
randomized evidence that PSA screening is
ineffective at diminishing prostate cancer mortality.
However, we recently reported that PSA contami-
nation in the study was significantly higher than
previously recognized with close to 90% of control
subjects reporting testing during the trial,
rendering the study results uninterpretable.2
Therefore, the only high quality, randomized evi-
dence comes from ERSPC (European Randomized
Study of Screening for Prostate Cancer), which
demonstrated a clear mortality benefit to screening.
1052 DECLINE IN PROSTATE CANCER SCREENING BY PRIMARY CARE PHYSICIANS
Preventable prostate cancer deaths are likely to
become more common as a result of misguided rec-
ommendations against PSA screening based on over
interpretation of the PLCO findings.
While we agree wholeheartedly with the recom-
mendations to improve screening, we would also
add a few caveats based on some of our recent data.
Using regression discontinuity, a quasi-experi-
mental statistical approach, we observed that bi-
opsy at a PSA cutoff of 4.0 ng/ml does not decrease
prostate cancer specific mortality or increase the
detection of high risk disease.3 While there is evi-
dence for numerous biopsy thresholds, our data do
REFERENCES
1. Andriole GL, Crawford ED, Grubb RL 3rd et al:
Prostate cancer screening in the randomized
Prostate, Lung, Colorectal, and Ovarian
Cancer Screening Trial: mortality results after
13 years of follow-up. J Natl Cancer Inst 2012;
104: 125.
not support the commonly used cutoff of PSA 4.0 ng/
ml to determine the need for prostate biopsy. This is
likely because a discrete cutoff is oversimplified and
does not maximize benefit, particularly in older
patients, and a more personalized screening
schedule and biopsy cutoff may be advantageous.
Additionally, we scrutinized prostate cancer mor-
tality in a cohort rigorously screened for prostate
cancer and found that men who ultimately died of
prostate cancer were older (median age 66 years)
when regular screening was initiated. This con-
tributes to the evidence demonstrating the benefit of
targeting younger men for PSA screening.4
2. Shoag J, Mittal S and Hu JC: Reevaluating PSA regression discontinuity in the PLCO Cancer
testing rates in the PLCO trial. N Engl J Med Screening Trial. JAMA Oncol 2015; 1: 984.
2016; 374: 1795.
4. Shoag J, Mittal S, Halpern JA et al: Lethal
3. Shoag J, Halpern J, Eisner B et al: Efficacy prostate cancer in the PLCO cancer screening trial.
of prostate-specific antigen screening: use of Eur Urol 2016; 70: 2.