Obstacles in prostate cancer screening: Current issues and future solutions

Abstract

Prostate cancer is the most common cancer in men and is associated with unacceptably high mortality rates, yet an accurate and acceptable screening programme that detects clinically significant prostate cancer remains elusive. Although there is good evidence that prostate-specific antigen (PSA)-based screening lowers prostate cancer-specific mortality, especially when conducted at high intensity, the harm caused by overinvestigation, overdiagnosis and overtreatment of clinically insignificant cases arguably outweighs these benefits. Several attempts have therefore been made to improve screening, enhancing the diagnostic value of PSA and identifying novel modalities for screening. Here, we provide a comprehensive review of the benefits and harms, and analyse which of these novel screening methods show most promise.

Level of evidence: 5, expert opinion

Keywords

Prostate cancer screening PSA prostatectomy MRI elastography

Get full access to this article

View all access options for this article.

References

Office for National Statistics. Cancer registration statistics - England, https://www.ons.gov.uk/peoplepopulationandcommunity/healthandsocialcare/conditionsanddiseases/bulletins/cancerregistrationstatisticsengland/final2016 (2016, accessed 25 August 2018).

Lloyd

Hounsome

Mehay

et al . Lifetime risk of being diagnosed with, or dying from, prostate cancer by major ethnic group in England 2008–2010. BMC Med; 13: 171.

Mariotto

Etzioni

Krapcho

et al . Reconstructing PSA testing patterns between black and white men in the US from Medicare claims and the National Health Interview Survey. Cancer 2007; 109: 1877–1886.

World Health Organization, Wilson

JMG

Jungner

Principles and practice of screening for disease, http://apps.who.int/iris/handle/10665/37650 (1968, accessed 2 September 2018).

U.S. Preventive Services Task Force. Final Update Summary: Prostate Cancer: Screening, 2008, https://www.uspreventiveservicestaskforce.org/Page/Document/UpdateSummaryFinal/prostate-cancer-screening-2008 (2008, accessed 9 September 2018).

U.S. Preventive Services Task Force. Final Update Summary: Prostate Cancer: Screening, https://www.uspreventiveservicestaskforce.org/Page/Document/UpdateSummaryFinal/prostate-cancer-screening (2012, accessed 9 September 2018).

U.S. Preventive Services Task Force. Final Recommendation Statement: Prostate Cancer: Screening, https://www.uspreventiveservicestaskforce.org/Page/Document/RecommendationStatementFinal/prostate-cancer-screening1 (2018, accessed 9 September 2018).

National Cancer Research Institute. Prostate Cancer Clinical Studies Group, https://csg.ncri.org.uk/about-the-csgs/clinical-studies-groups/prostate/ (2018, accessed 17 September 2018).

Collin

Martin

Metcalfe

et al . Prostate-cancer mortality in the USA and UK in 1975–2004: An ecological study. Lancet Oncol 2008; 9: 445–452.

10.

Bartsch

Horninger

Klocker

et al . Prostate cancer mortality after introduction of prostate-specific antigen mass screening in the Federal State of Tyrol, Austria. Urology 2001; 58: 417–424.

11.

Andriole

Crawford

Grubb

et al . Mortality results from a randomized prostate-cancer screening trial. N Engl J Med 2009; 360: 1310–1319.

12.

Andriole

Crawford

Grubb

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: 125–132.

13.

Schröder

Hugosson

Roobol

et al . Screening and prostate-cancer mortality in a randomized European study. N Engl J Med 2009; 360: 1320–1328.

14.

Schröder

Hugosson

Roobol

et al . Screening and prostate cancer mortality: Results of the European Randomised Study of Screening for Prostate Cancer (EPSRC) at 13 Years of Follow-up. Lancet 2014; 384: 2027–2035.

15.

Shoag

Mittal

JC.

Reevaluating PSA testing rates in the PLCO Trial. N Engl J Med 2016; 374: 1795–1796.

16.

Barry

MJ.

Screening for prostate cancer–the controversy that refuses to die. N Engl J Med 2009; 360: 1351–1354.

17.

Tsodikov

Gulati

Heijnsdijk

EAM

et al . Reconciling the effects of screening on prostate cancer mortality in the ERSPC and PLCO trials. Ann Intern Med 2017; 167: 449–455.

18.

Hugosson

Carlsson

Aus

et al . Mortality results from the Göteborg randomised population-based prostate-cancer screening trial. Lancet Oncol 2010; 11: 725–732.

19.

Alpert

PF.

New evidence for the benefit of prostate-specific antigen screening: Data from 400,887 Kaiser Permanente patients. Urology 2018; 118: 119–126.

20.

Martin

Donovan

Turner

et al . Effect of a low-intensity PSA-based screening intervention on prostate cancer mortality: The CAP randomized clinical trial. JAMA 2018; 319: 883–895.

21.

Jahn

Giovannucci

Stampfer

MJ.

The high prevalence of undiagnosed prostate cancer at autopsy: Implications for epidemiology and treatment of prostate cancer in the prostate-specific antigen-era. Int J Cancer 2015; 137: 2795–2802.

22.

Welch

Albertsen

PC.

Prostate cancer diagnosis and treatment after the introduction of prostate-specific antigen screening: 1986–2005. J Natl Cancer Inst 2009; 101: 1325–1329.

23.

Alibhai

SMH

Leach

Tomlinson

et al . 30-day mortality and major complications after radical prostatectomy: Influence of age and comorbidity. J Natl Cancer Inst 2005; 97: 1525–1532.

24.

Sanda

Dunn

Michalski

et al . Quality of life and satisfaction with outcome among prostate-cancer survivors. N Engl J Med 2008; 358: 1250–1261.

25.

Kundu

Roehl

Eggener

et al . Potency, continence and complications in 3,477 consecutive radical retropubic prostatectomies. J Urol 2004; 172: 2227–2231.

26.

Elliott

Meng

Elkin

et al . Incidence of urethral stricture after primary treatment for prostate cancer: Data From CaPSURE. J Urol 2007; 178: 529–534; discussion 534.

27.

Bancroft

Page

Castro

et al . Targeted prostate cancer screening in BRCA1 and BRCA2 mutation carriers: Results from the initial screening round of the IMPACT study. Eur Urol 2014; 66: 489–499.

28.

Gudmundsson

Besenbacher

Sulem

et al . Genetic correction of PSA values using sequence variants associated with PSA levels. Sci Transl Med 2010; 2: 62ra92.

29.

Tricoli

Schoenfeldt

Conley

BA.

Detection of prostate cancer and predicting progression: Current and future diagnostic markers. Clin Cancer Res 2004; 10: 3943–3953.

30.

Roobol

Schröder

van Leeuwen

et al . Performance of the prostate cancer antigen 3 (PCA3) gene and prostate-specific antigen in prescreened men: Exploring the value of PCA3 for a first-line diagnostic test. Eur Urol 2010; 58: 475–481.

31.

Vlaeminck-Guillem

Ruffion

André

et al . Urinary prostate cancer 3 test: Toward the age of reason? Urology 2010; 75: 447–453.

32.

Vickers

Savage

O’Brien

et al . Systematic review of pretreatment prostate-specific antigen velocity and doubling time as predictors for prostate cancer. J Clin Oncol 2009; 27: 398–403.

33.

Bryant

Sjoberg

Vickers

et al . Predicting high-grade cancer at ten-core prostate biopsy using four kallikrein markers measured in blood in the ProtecT study. J Natl Cancer Inst. Epub ahead of print July 2015. DOI: 10.1093/jnci/djv095.

34.

Parekh

Punnen

Sjoberg

et al . A multi-institutional prospective trial in the USA confirms that the 4Kscore accurately identifies men with high-grade prostate cancer. Eur Urol 2015; 68: 464–470.

35.

Stattin

Vickers

Sjoberg

et al . Improving the specificity of screening for lethal prostate cancer using prostate-specific antigen and a panel of kallikrein markers: A nested case-control study. Eur Urol 2015; 68: 207–213.

36.

Grönberg

Adolfsson

Aly

et al . Prostate cancer screening in men aged 50–69 years (STHLM3): A prospective population-based diagnostic study. Lancet Oncol 2015; 16: 1667–1676.

37.

Vourganti

Rastinehad

Yerram

et al . Multiparametric magnetic resonance imaging and ultrasound fusion biopsy detect prostate cancer in patients with prior negative transrectal ultrasound biopsies. J Urol 2012; 188: 2152–2157.

38.

Abd-Alazeez

Kirkham

Ahmed

et al . Performance of multiparametric MRI in men at risk of prostate cancer before the first biopsy: A paired validating cohort study using template prostate mapping biopsies as the reference standard. Prostate Cancer Prostatic Dis 2014; 17: 40–46.

39.

Weaver

Kim

Vetter

et al . Presence of magnetic resonance imaging suspicious lesion predicts Gleason 7 or greater prostate cancer in biopsy-naive patients. Urology 2016; 88: 119–124.

40.

Grenabo Bergdahl

Wilderäng

Aus

et al . Role of magnetic resonance imaging in prostate cancer screening: A pilot study within the Göteborg randomised screening trial. Eur Urol 2016; 70: 566–573.

41.

Salami

Vira

Turkbey

et al . Multiparametric magnetic resonance imaging outperforms the Prostate Cancer Prevention Trial risk calculator in predicting clinically significant prostate cancer. Cancer 2014; 120: 2876–2882.

42.

Ahmed

Bosaily

AE-S

Brown

et al . Diagnostic accuracy of multi-parametric MRI and TRUS biopsy in prostate cancer (PROMIS): A paired validating confirmatory study. Lancet 2017; 389: 815–822.

43.

Kasivisvanathan

Rannikko

Borghi

et al . MRI-targeted or standard biopsy for prostate-cancer diagnosis. N Engl J Med 2018; 378: 1767–1777.

44.

Phipps

Yang

THJ

Habib

et al . Measurement of tissue mechanical characteristics to distinguish between benign and malignant prostatic disease. Urology 2005; 66: 447–450.

45.

Itoh

Ueno

Tohno

et al . Breast disease: Clinical application of US elastography for diagnosis. Radiology 2006; 239: 341–350.

46.

Lyshchik

Higashi

Asato

et al . Thyroid gland tumor diagnosis at US elastography. Radiology 2005; 237: 202–211.

47.

Barr

Memo

Schaub

CR.

Shear wave ultrasound elastography of the prostate: Initial results. Ultrasound Q 2012; 28: 13–20.

48.

Sang

Wang

et al . Accuracy of shear wave elastography for the diagnosis of prostate cancer: A meta-analysis. Sci Rep 2017; 7: 1949.

49.

Wei

Szewczyk-Bieda

et al . Performance characteristics of transrectal shear wave elastography imaging in the evaluation of clinically localized prostate cancer: A prospective study. J Urol 2018; 200: 549–558.

50.

University College London. REIMAGINE Trial Information, https://www.ucl.ac.uk/surgery/research/situ-trials/reimagine/reimagine-trial-information (2018, accessed 17 September 2018).