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Effect of a Low-Intensity PSA-Based Screening Intervention on Prostate Cancer MortalityThe CAP Randomized Clinical Trial

Educational Objective
To learn whether a prostate cancer screening strategy decreased prostate cancer mortality.
1 Credit CME
Key Points

Question  What is the effect of an invitation to a single prostate-specific antigen (PSA) screening on prostate cancer detection and median 10-year prostate cancer mortality?

Findings  In this randomized clinical trial comparing men aged 50 to 69 years undergoing a single PSA screening (n = 189 386) vs controls not undergoing a PSA screening (n = 219 439), the proportion of men diagnosed with prostate cancer was higher in the intervention group (4.3%) than in the control group (3.6%); however, there was no significant difference in prostate cancer mortality (0.30 per 1000 person-years for the intervention group vs 0.31 for the control group) after a median follow-up of 10 years.

Meaning  The single PSA screening intervention detected more prostate cancer cases but had no significant effect on prostate cancer mortality after a median follow-up of 10 years.

Abstract

Importance  Prostate cancer screening remains controversial because potential mortality or quality-of-life benefits may be outweighed by harms from overdetection and overtreatment.

Objective  To evaluate the effect of a single prostate-specific antigen (PSA) screening intervention and standardized diagnostic pathway on prostate cancer–specific mortality.

Design, Setting, and Participants  The Cluster Randomized Trial of PSA Testing for Prostate Cancer (CAP) included 419 582 men aged 50 to 69 years and was conducted at 573 primary care practices across the United Kingdom. Randomization and recruitment of the practices occurred between 2001 and 2009; patient follow-up ended on March 31, 2016.

Intervention  An invitation to attend a PSA testing clinic and receive a single PSA test vs standard (unscreened) practice.

Main Outcomes and Measures  Primary outcome: prostate cancer–specific mortality at a median follow-up of 10 years. Prespecified secondary outcomes: diagnostic cancer stage and Gleason grade (range, 2-10; higher scores indicate a poorer prognosis) of prostate cancers identified, all-cause mortality, and an instrumental variable analysis estimating the causal effect of attending the PSA screening clinic.

Results  Among 415 357 randomized men (mean [SD] age, 59.0 [5.6] years), 189 386 in the intervention group and 219 439 in the control group were included in the analysis (n = 408 825; 98%). In the intervention group, 75 707 (40%) attended the PSA testing clinic and 67 313 (36%) underwent PSA testing. Of 64 436 with a valid PSA test result, 6857 (11%) had a PSA level between 3 ng/mL and 19.9 ng/mL, of whom 5850 (85%) had a prostate biopsy. After a median follow-up of 10 years, 549 (0.30 per 1000 person-years) died of prostate cancer in the intervention group vs 647 (0.31 per 1000 person-years) in the control group (rate difference, −0.013 per 1000 person-years [95% CI, −0.047 to 0.022]; rate ratio [RR], 0.96 [95% CI, 0.85 to 1.08]; P = .50). The number diagnosed with prostate cancer was higher in the intervention group (n = 8054; 4.3%) than in the control group (n = 7853; 3.6%) (RR, 1.19 [95% CI, 1.14 to 1.25]; P < .001). More prostate cancer tumors with a Gleason grade of 6 or lower were identified in the intervention group (n = 3263/189 386 [1.7%]) than in the control group (n = 2440/219 439 [1.1%]) (difference per 1000 men, 6.11 [95% CI, 5.38 to 6.84]; P < .001). In the analysis of all-cause mortality, there were 25 459 deaths in the intervention group vs 28 306 deaths in the control group (RR, 0.99 [95% CI, 0.94 to 1.03]; P = .49). In the instrumental variable analysis for prostate cancer mortality, the adherence-adjusted causal RR was 0.93 (95% CI, 0.67 to 1.29; P = .66).

Conclusions and Relevance  Among practices randomized to a single PSA screening intervention vs standard practice without screening, there was no significant difference in prostate cancer mortality after a median follow-up of 10 years but the detection of low-risk prostate cancer cases increased. Although longer-term follow-up is under way, the findings do not support single PSA testing for population-based screening.

Trial Registration  ISRCTN Identifier: ISRCTN92187251

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Article Information

Corresponding Author: Richard M. Martin, PhD, University of Bristol, Canynge Hall, 39 Whatley Rd, Bristol BS8 2PS, England (richard.martin@bristol.ac.uk).

Accepted for Publication: January 17, 2018.

Author Contributions: Drs Martin and Metcalfe had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Drs Martin, Donovan, Turner, Metcalfe, Neal, and Hamdy contributed equally.

Concept and design: Martin, Donovan, Turner, Noble, Oliver, Evans, Sterne, Ben-Shlomo, Brindle, Davey Smith, Neal, Hamdy.

Acquisition, analysis, or interpretation of data: Martin, Donovan, Turner, Metcalfe, Young, Walsh, Lane, Noble, Oliver, Evans, Sterne, Holding, Williams, Hill, Ng, Toole, Tazewell, Hughes, Davies, Thorn, Down.

Drafting of the manuscript: Martin, Donovan, Turner, Young, Sterne, Hamdy.

Critical revision of the manuscript for important intellectual content: Martin, Donovan, Turner, Metcalfe, Young, Walsh, Lane, Noble, Oliver, Evans, Sterne, Holding, Ben-Shlomo, Brindle, Williams, Hill, Ng, Toole, Tazewell, Hughes, Davies, Thorn, Down, Davey Smith, Neal.

Statistical analysis: Martin, Turner, Metcalfe, Young, Walsh, Oliver, Sterne.

Obtained funding: Martin, Donovan, Turner, Noble, Oliver, Sterne, Neal, Hamdy.

Administrative, technical, or material support: Donovan, Turner, Walsh, Lane, Williams, Hill, Ng, Toole, Hughes, Davies, Thorn, Down.

Supervision: Martin, Turner, Noble, Evans, Sterne, Ben-Shlomo, Williams.

Conflict of Interest Disclosures: The authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest and none were reported.

Funding/Support: The CAP trial was funded by grants C11043/A4286, C18281/A8145, C18281/A11326, and C18281/A15064 from Cancer Research UK. The UK Department of Health, National Institute of Health Research provided partial funding. The ProtecT trial was funded by project grants 96/20/06 and 96/20/99 from the UK National Institute for Health Research, Health Technology Assessment Programme. The National Institute for Health Research Oxford Biomedical Research Centre provided support through the Surgical Innovation and Evaluation Theme and the Surgical Interventional Trials Unit and Cancer Research UK through the Oxford Cancer Research Centre. Drs Martin and Sterne are supported in part by the National Institute for Health Research Bristol Biomedical Research Centre. Drs Donovan and Ben-Shlomo are supported in part by the National Institute for Health Research Collaboration for Leadership in Applied Health Research and Care West. Ms Young and Dr Lane are supported in part by the Bristol Randomized Trials Collaboration.

Role of the Funder/Sponsor: The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Group Information: The CAP Trial Group members are Richard Martin (lead primary investigator), Jenny Donovan (primary investigator), David Neal (primary investigator), Freddie Hamdy (primary investigator), Emma Turner (trial coordinator), Chris Metcalfe (statistician), J. Athene Lane (ProtecT trial coordinator), Jonathan Sterne (statistician), Sian Noble (health economist), and Stephen Frankel (retired epidemiologist). The ProtecT trial group members are Prasad Bollina, MBBS (Department of Urology and Surgery, Western General Hospital, University of Edinburgh), James Catto, PhD (Academic Urology Unit, University of Sheffield), Andrew Doble, MS (Department of Urology, Addenbrooke’s Hospital, Cambridge), Alan Doherty, MBBS (Department of Urology, Queen Elizabeth Hospital, Birmingham), David Gillatt, MS (Bristol Urological Institute, Southmead Hospital, Bristol), Vincent Gnanapragasam, MBBS (Department of Surgery, Addenbrooke’s Hospital, Cambridge), Peter Holding, MSc (Nuffield Department of Surgical Sciences, University of Oxford, Oxford), Owen Hughes, DM (Department of Urology, Cardiff and Vale University Health Board, Cardiff), Roger Kockelbergh, MD (Department of Urology, University Hospitals of Leicester, Leicester), Howard Kynaston, MD (Department of Urology, Cardiff and Vale University Health Board, Cardiff), Alan Paul, MD (Department of Urology, Leeds Teaching Hospitals NHS Trust, Leeds), Edgar Paez, MBBS (Department of Urology, Freeman Hospital, Newcastle-upon-Tyne), Derek J. Rosario, MD (Academic Urology Unit, University of Sheffield, Sheffield), and Edward Rowe, MD (Bristol Urological Institute, Southmead Hospital, Bristol). The management committee: Emma Turner (chair), Richard Martin, Jenny Donovan, Chris Metcalfe, Jonathan Sterne, Sian Noble, Yoav Ben-Shlomo, J. Athene Lane, Steven Oliver, Peter Brindle, and Simon Evans.

Disclaimer: The views expressed in this article are those of the authors and do not necessarily reflect the opinions of the National Health Service, the National Institute for Health Research, or the Department of Health. The Office of National Statistics bears no responsibility for the analysis and interpretation of the data provided.

Additional Contributions: We acknowledge the work of the research staff: Elizabeth Hill, Siaw Yein Ng, Naomi Williams, Elizabeth Down (data manager), Eleanor Walsh (data manager), Jessica Toole, Marta Tazewell (data), Pete Shiarly (database developer), Joanna Thorn (health economist), Charlotte Davies, Laura Hughes, Mari-Anne Rowlands, and Lindsey Bell; the trial steering committee: Michael Baum (chair), Peter Albertsen, Tracy Roberts, Mary Robinson, Jan Adolfsson, David Dearnaley, Anthony Zietman, Fritz Schröder, Tim Peters, Peter Holding, Teresa Lennon, Sue Bonnington, Malcolm Mason, Jon Oxley, Richard Martin, Jenny Donovan, David Neal, Freddie Hamdy, Emma Turner, and J. Athene Lane; the data monitoring committee: Lars Holmberg (chair), Robert Pickard, Simon Thompson, and Usha Menon; the cause of death committee: Peter Albertsen (chair), Colette Reid, Jon McFarlane, Jon Oxley, Mary Robinson, Jan Adolfsson, Michael Baum, Anthony Zietman, Amit Bahl, Anthony Koupparis, and David Gunnell; and the expert attendees at a discussion workshop in March 2017 to consider the implications of the trial results: Jan Adolfsson, PhD (Karolinska Institutet), Peter Albertsen, MD (University of Connecticut), Mike Baum, ChM (University College London-honorary), Lucy Davies, PhD (Cancer Research UK), Harry De Koning, PhD (Erasmus Medical Centre), Jenny Donovan, PhD (University of Bristol), Ruth Etzioni, PhD (Fred Hutchinson Cancer Research Center), Simon Evans, MD (Royal United Hospital Bath NHS Foundation Trust), Roman Gulati, MS (Fred Hutchinson Cancer Research Center), Freddie Hamdy, MD (University of Oxford), Peter Holding, MSc (Nuffield Department of Surgical Sciences, University of Oxford, Oxford), Lars Holmberg, PhD (Kings College London), Jonas Hugosson, PhD (University of Gothenburg), J. Athene Lane, PhD (University of Bristol), Richard Martin, PhD (University of Bristol), Malcolm Mason, MD (University of Cardiff), Jon McFarlane, MS (Royal United Hospitals Bath), Chris Metcalfe, PhD (University of Bristol), David Neal, MD (University of Oxford), Sian Noble, PhD (University of Bristol), Steven Oliver, PhD (University of York), Jon Oxley, MD (North Bristol NHS Trust), Nora Pashayan, PhD (University College London), Mary Robinson, MBBS (Royal Victoria Infirmary), Sabina Sanghera, PhD (University of Bristol), Fritz Schroder, PhD (University Medical Center Rotterdam), Emma Turner, PhD (University of Bristol), Grace Young, MSc (University of Bristol), and Anthony Zietman, MD (Massachusetts General Hospital). We are extremely grateful to Jan Adolfsson, Peter Albertsen, and Anthony Zietman who provided insightful comments on the manuscript. The attendees at the workshop received reimbursement for travel expenses but were not otherwise compensated for their role in the study. We acknowledge the contribution of all members of the ProtecT trial research group and especially the following: Sue Bonnington, RGN (Leicester General Hospital, Leicester), Lynne Bradshaw, RGN (Southmead Hospital, Bristol), Debbie Cooper, RGN (St James Hospital, Leeds), Garrett Durkan, MD (Freeman Hospital, Newcastle), Emma Elliott, RGN (Southmead Hospital, Bristol), Pippa Herbert, RGN (Addenbrook’s Hospital, Cambridge), Joanne Howson, RGN (Royal Hallamshire Hospital, Sheffield), Mandy Jones, RGN (University Hospital Wales, Cardiff), Teresa Lennon, RGN (Freeman Hospital, Newcastle), Norma Lyons, RGN (Western General Hospital, Edinburgh), Hing Leung, PhD, FRCS (University of Glasgow), Malcolm Mason, MD (University of Cardiff, Cardiff), Hilary Moody, RGN (Southmead Hospital, Bristol), Philip Powell, MD (Freeman Hospital, Newcastle), Stephen Prescott, MD (St James Hospital, Leeds), Patricia O'Sullivan, RGN (Southmead Hospital, Bristol), Pauline Thompson, RGN (Queen Elizabeth Hospital, Birmingham), Sarah Tidball, RGN (University Hospital Wales, Cardiff), Liz Salter, RGN (Southmead Hospital, Bristol), Jan Blaikie, RGN (Western General Hospital, Edinburgh), Catherine Gray, RGN (St James Hospital, Leeds), Sarah Hawkins, RGN (University Hospital Wales, Cardiff), Michael Slater, RGN (Royal Hallamshire Hospital, Sheffield), and Sue Kilner, RGN (Royal Hallamshire Hospital, Sheffield). None of the ProtecT trial research group received compensation for their role in the study. We acknowledge the administrative staff: Chris Pawsey and Genevieve Hatton-Brown (both employed by the CAP trial and were compensated) and Tom Steuart-Feilding (employed by the ProtecT trial and did not receive compensation for his role in the study). We also acknowledge the work of the NHS Digital Organization, Office of National Statistics, and Public Health Wales and Public Health England National Cancer Registration and Analysis Service (South West) for their assistance with this study, in particular Julia Verne, PhD (Public Health England), Luke Hounsome, PhD (Public Health England), Isobel Tudge, MSc (Public Health England), and Tariq Malik, MSc (Public Health England); none of these individuals received compensation for their role in the study. We also acknowledge the contribution of all the CAP and ProtecT study participants and the CAP trial general practioners and practice staff.

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