Prostate cancer screening in Switzerland: a literature review and consensus statement from the Swiss Society of Urology (original) (raw)

Review article: Biomedical intelligence

Vol. 154 No. 5 (2024)

Summary

Over a decade ago, the United States Preventive Services Taskforce (USPSTF) recommended against prostate-specific antigen (PSA)-based screening for prostate cancer in all men, which considerably influenced prostate cancer screening policies worldwide after that. Consequently, the world has seen increasing numbers of advanced stages and prostate cancer deaths, which later led the USPSTF to withdraw its initial statement. Meanwhile, the European Union has elaborated a directive to address the problem of implementing prostate cancer screening in “Europe’s Beating Cancer Plan”. In Switzerland, concerned urologists formed an open Swiss Prostate Cancer Screening Group to improve the early detection of prostate cancer. On the 20th of September 2023, during the annual general assembly of the Swiss Society of Urology (SGU/SSU) in Lausanne, members positively voted for a stepwise approach to evaluate the feasibility of implementing organised prostate cancer screening programs in Switzerland. The following article will summarise the events and scientific advances in the last decade during which evidence and promising additional modalities to complement PSA-based prostate cancer screening have emerged. It also aims to provide an overview of contemporary strategies and their potential harms and benefits.

References

  1. Moyer VA; U.S. Preventive Services Task Force. Screening for prostate cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2012 Jul;157(2):120–34. 10.7326/0003-4819-157-2-201207170-00459 DOI: https://doi.org/10.7326/0003-4819-157-2-201207170-00459
  2. Jemal A, Culp MB, Ma J, Islami F, Fedewa SA. Prostate Cancer Incidence 5 Years After US Preventive Services Task Force Recommendations Against Screening. J Natl Cancer Inst. 2021 Jan;113(1):64–71. 10.1093/jnci/djaa068 DOI: https://doi.org/10.1093/jnci/djaa068
  3. Welch HG, Albertsen PC. Reconsidering Prostate Cancer Mortality — The Future of PSA Screening. Malina D, editor. N Engl J Med. 2020 Apr 16;382(16):1557–63. DOI: https://doi.org/10.1056/NEJMms1914228
  4. Siegel RL, Miller KD, Wagle NS, Jemal A. Cancer statistics, 2023. CA Cancer J Clin. 2023 Jan;73(1):17–48. 10.3322/caac.21763 DOI: https://doi.org/10.3322/caac.21763
  5. Desai MM, Cacciamani GE, Gill K, Zhang J, Liu L, Abreu A, et al. Trends in Incidence of Metastatic Prostate Cancer in the US. JAMA Netw Open. 2022 Mar;5(3):e222246. 10.1001/jamanetworkopen.2022.2246 DOI: https://doi.org/10.1001/jamanetworkopen.2022.2246
  6. Grossman DC, Curry SJ, Owens DK, Bibbins-Domingo K, Caughey AB, Davidson KW, et al.; US Preventive Services Task Force. Screening for Prostate Cancer: US Preventive Services Task Force Recommendation Statement. JAMA. 2018 May;319(18):1901–13. 10.1001/jama.2018.3710 DOI: https://doi.org/10.1001/jama.2018.3710
  7. Weiner AB, Matulewicz RS, Eggener SE, Schaeffer EM. Increasing incidence of metastatic prostate cancer in the United States (2004-2013). Prostate Cancer Prostatic Dis. 2016 Dec;19(4):395–7. 10.1038/pcan.2016.30 DOI: https://doi.org/10.1038/pcan.2016.30
  8. Council Recommendation on strengthening prevention through early detection: A new EU approach on cancer screening replacing Council Recommendation 2003/878/EC. Available from: https://ec.europa.eu/commission/presscorner/detail/en/ip_22_7548
  9. Rao AR, Motiwala HG, Karim OM. The discovery of prostate-specific antigen. BJU Int. 2007 Aug. DOI: https://doi.org/10.1111/j.1464-410X.2007.07138.x
  10. Catalona WJ, Smith DS, Ratliff TL, Dodds KM, Coplen DE, Yuan JJ, et al. Measurement of prostate-specific antigen in serum as a screening test for prostate cancer. N Engl J Med. 1991 Apr;324(17):1156–61. 10.1056/NEJM199104253241702 DOI: https://doi.org/10.1056/NEJM199104253241702
  11. Schröder FH, Hugosson J, Roobol MJ, Tammela TL, Ciatto S, Nelen V, et al.; ERSPC Investigators. Screening and prostate-cancer mortality in a randomized European study. N Engl J Med. 2009 Mar;360(13):1320–8. 10.1056/NEJMoa0810084 DOI: https://doi.org/10.1056/NEJMoa0810084
  12. Andriole GL, Crawford ED, Grubb RL 3rd, Buys SS, Chia D, Church TR, et al.; PLCO Project Team. Mortality results from a randomized prostate-cancer screening trial. N Engl J Med. 2009 Mar;360(13):1310–9. 10.1056/NEJMoa0810696 DOI: https://doi.org/10.1056/NEJMoa0810696
  13. Andriole GL, Crawford ED, Grubb RL 3rd, Buys SS, Chia D, Church TR, et al.; PLCO Project Team. 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 Jan;104(2):125–32. 10.1093/jnci/djr500 DOI: https://doi.org/10.1093/jnci/djr500
  14. Pinsky PF, Parnes HL, Andriole G. Mortality and complications after prostate biopsy in the Prostate, Lung, Colorectal and Ovarian Cancer Screening (PLCO) trial. BJU Int. 2014 Feb;113(2):254–9. 10.1111/bju.12368 DOI: https://doi.org/10.1111/bju.12368
  15. Swiss Medical Board (SMB). Stellenwert des PSA-Wertes bei der Früherkennung des Prostatakarzinoms. Health Technology Assessment Report. Available from: https://www.swissmedicalboard.ch
  16. Gasser T, Iselin C, Jichlinksi P, Kreienbühl B, Merz V, Recker F, et al. PSA-Bestimmung ‒ Empfehlungen der Schweizerischen Gesellschaft für Urologie (SGU). Swiss Med Forum ‒ Schweizerisches Medizin-Forum. 2012 Feb 8;12(06). DOI: https://doi.org/10.4414/smf.2012.07772
  17. Mottet N, Cornford P, Van den Bergh R, et al. EAU - EANM - ESTRO - ESUR - ISUP - SIOG Guidelines on Prostate Cancer 2023. European Association of Urology Guidelines. 2023 Edition. Arnhem, The Netherlands: European Association of Urology Guidelines Office; 2023., Available from https://uroweb.org/guidelines/prostate-cancer
  18. Wei JT, Barocas D, Carlsson S, Coakley F, Eggener S, Etzioni R, et al. Early Detection of Prostate Cancer: AUA/SUO Guideline Part I: Prostate Cancer Screening. J Urol. 2023 Jul;210(1):46–53. 10.1097/JU.0000000000003491 DOI: https://doi.org/10.1097/JU.0000000000003491
  19. Cooperberg MR. Prostate cancer: why the prostate arm of the PLCO trial failed and what it has taught us. Nat Rev Urol. 2016 Aug;13(8):439–40. 10.1038/nrurol.2016.116 DOI: https://doi.org/10.1038/nrurol.2016.116
  20. Shoag JE, Mittal S, Hu JC. Reevaluating PSA Testing Rates in the PLCO Trial. N Engl J Med. 2016 May;374(18):1795–6. 10.1056/NEJMc1515131 DOI: https://doi.org/10.1056/NEJMc1515131
  21. Pinsky PF, Andriole GL, Kramer BS, Hayes RB, Prorok PC, Gohagan JK; Prostate, Lung, Colorectal and Ovarian Project Team. Prostate biopsy following a positive screen in the prostate, lung, colorectal and ovarian cancer screening trial. J Urol. 2005 Mar;173(3):746–50. 10.1097/01.ju.0000152697.25708.71 DOI: https://doi.org/10.1097/01.ju.0000152697.25708.71
  22. Pinsky PF, Prorok PC, Yu K, Kramer BS, Black A, Gohagan JK, et al. Extended mortality results for prostate cancer screening in the PLCO trial with median follow-up of 15 years. Cancer. 2017 Feb;123(4):592–9. 10.1002/cncr.30474 DOI: https://doi.org/10.1002/cncr.30474
  23. Schröder FH, Hugosson J, Roobol MJ, Tammela TL, Zappa M, Nelen V, et al.; ERSPC Investigators. Screening and prostate cancer mortality: results of the European Randomised Study of Screening for Prostate Cancer (ERSPC) at 13 years of follow-up. Lancet. 2014 Dec;384(9959):2027–35. 10.1016/S0140-6736(14)60525-0 DOI: https://doi.org/10.1016/S0140-6736(14)60525-0
  24. Hugosson J, Roobol MJ, Månsson M, Tammela TL, Zappa M, Nelen V, et al.; ERSPC investigators. A 16-yr Follow-up of the European Randomized study of Screening for Prostate Cancer. Eur Urol. 2019 Jul;76(1):43–51. 10.1016/j.eururo.2019.02.009
  25. Schröder FH, Hugosson J, Carlsson S, Tammela T, Määttänen L, Auvinen A, et al. Screening for prostate cancer decreases the risk of developing metastatic disease: findings from the European Randomized Study of Screening for Prostate Cancer (ERSPC). Eur Urol. 2012 Nov;62(5):745–52. 10.1016/j.eururo.2012.05.068 DOI: https://doi.org/10.1016/j.eururo.2012.05.068
  26. Bretthauer M, Løberg M, Wieszczy P, Kalager M, Emilsson L, Garborg K, et al.; NordICC Study Group. Effect of Colonoscopy Screening on Risks of Colorectal Cancer and Related Death. N Engl J Med. 2022 Oct;387(17):1547–56. 10.1056/NEJMoa2208375 DOI: https://doi.org/10.1056/NEJMoa2208375
  27. Gøtzsche PC, Nielsen M. Screening for breast cancer with mammography. Cochrane Database Syst Rev. 2006 Oct 18;(4):CD001877. doi: 10.1002/14651858.CD001877.pub2. Update in: Cochrane Database Syst Rev. 2009;(4):CD001877. PMID: 17054145. 10.1002/14651858.CD001877.pub3
  28. Draft for Update of USPSTF Statement on Prostate Cancer Screening. Available from: https://www.uspreventiveservicestaskforce.org/uspstf/draft-update-summary/prostate-cancer-screening-adults
  29. Jungblut L, von Garnier C, Puhan M, Tomonaga Y, Kaufmann C, Azzola A, et al. The Swiss Approach - feasibility of a national low-dose CT lung cancer screening program. Swiss Med Wkly. 2022 Apr;152(15-16):w30154. 10.4414/SMW.2022.w30154 DOI: https://doi.org/10.4414/SMW.2022.w30154
  30. Proposal for a Council Recommendation on strengthening prevention through early detection: A new EU approach on cancer screening replacing Council Recommendation 2003/878/EC. Available from: https://health.ec.europa.eu/system/files/2022-09/com_2022-474_annex_en.pdf
  31. Bratt O, Godtman RA, Jiborn T, Wallström J, Akre O, Carlsson S, et al. Population-based Organised Prostate Cancer Testing: Results from the First Invitation of 50-year-old Men. Eur Urol. 2024 Mar;85(3):207–14. 10.1016/j.eururo.2023.11.013 DOI: https://doi.org/10.1016/j.eururo.2023.11.013
  32. Swedish Organised Prostate Cancer Testing (OPT). Available from: https://cancercentrum.se/samverkan/vara-uppdrag/prevention-och-tidig-upptackt/prostatacancertestning/organised-prostate-cancer-testing/
  33. Wurnschimmel C, Grande P, Moschini M, Ferrari M, Mordasini L, Mattei A. Accuracy of standardized 12-core template biopsies versus non-standardized biopsies for detection of Epstein Grade 5 prostate cancer regarding the histology of the prostatectomy specimen. Prostate . 2018/01/26. 2018;78(5):365–9. DOI: https://doi.org/10.1002/pros.23480
  34. Ulyte A, Wei W, Dressel H, Gruebner O, von Wyl V, Bähler C, et al. Variation of colorectal, breast and prostate cancer screening activity in Switzerland: Influence of insurance, policy and guidelines. Van Hemelrijck M, editor. PLoS One. 2020 Apr 16;15(4):e0231409. DOI: https://doi.org/10.1371/journal.pone.0231409
  35. Guessous I, Cullati S, Fedewa SA, Burton-Jeangros C, Courvoisier DS, Manor O, et al. Prostate cancer screening in Switzerland: 20-year trends and socioeconomic disparities. Prev Med. 2016 Jan;82:83–91. 10.1016/j.ypmed.2015.11.009 DOI: https://doi.org/10.1016/j.ypmed.2015.11.009
  36. Scherer TP, Saba K, Wettstein MS, Lucca I, Mortezavi A, Waisbrod S, et al. Do Swiss urologists and Swiss internists screen themselves and their relatives for prostate cancer? A questionnaire study. Swiss Med Wkly. 2023 Sep;153(9):40115. 10.57187/smw.2023.40115 DOI: https://doi.org/10.57187/smw.2023.40115
  37. Vickers A, O’Brien F, Montorsi F, Galvin D, Bratt O, Carlsson S, et al. Current policies on early detection of prostate cancer create overdiagnosis and inequity with minimal benefit. BMJ. 2023 May;381:e071082. 10.1136/bmj-2022-071082 DOI: https://doi.org/10.1136/bmj-2022-071082
  38. Shoag JE, Nyame YA, Gulati R, Etzioni R, Hu JC. Reconsidering the Trade-offs of Prostate Cancer Screening. N Engl J Med. 2020 Jun;382(25):2465–8. 10.1056/NEJMsb2000250 DOI: https://doi.org/10.1056/NEJMsb2000250
  39. Washington SL 3rd, Jeong CW, Lonergan PE, Herlemann A, Gomez SL, Carroll PR, et al. Regional Variation in Active Surveillance for Low-Risk Prostate Cancer in the US. JAMA Netw Open. 2020 Dec;3(12):e2031349. 10.1001/jamanetworkopen.2020.31349 DOI: https://doi.org/10.1001/jamanetworkopen.2020.31349
  40. Hogenhout R, Remmers S, van Leenders GJ, Roobol MJ. The transition from transrectal to transperineal prostate biopsy without antibiotic prophylaxis: cancer detection rates and complication rates. Prostate Cancer Prostatic Dis. 2023 Sep;26(3):581–7. 10.1038/s41391-022-00641-3 DOI: https://doi.org/10.1038/s41391-022-00641-3
  41. Kasivisvanathan V, Rannikko AS, Borghi M, Panebianco V, Mynderse LA, Vaarala MH, et al. MRI-Targeted or Standard Biopsy for Prostate-Cancer Diagnosis. N Engl J Med . 2018/03/20. 2018;378(19):1767–77. DOI: https://doi.org/10.1056/NEJMoa1801993
  42. Hugosson J, Månsson M, Wallström J, Axcrona U, Carlsson SV, Egevad L, et al.; GÖTEBORG-2 Trial Investigators. Prostate Cancer Screening with PSA and MRI Followed by Targeted Biopsy Only. N Engl J Med. 2022 Dec;387(23):2126–37. 10.1056/NEJMoa2209454 DOI: https://doi.org/10.1056/NEJMoa2209454
  43. Nordström T, Discacciati A, Bergman M, Clements M, Aly M, Annerstedt M, et al.; STHLM3 study group. Prostate cancer screening using a combination of risk-prediction, MRI, and targeted prostate biopsies (STHLM3-MRI): a prospective, population-based, randomised, open-label, non-inferiority trial. Lancet Oncol. 2021 Sep;22(9):1240–9. 10.1016/S1470-2045(21)00348-X
  44. Würnschimmel C, Chandrasekar T, Hahn L, Esen T, Shariat SF, Tilki D. MRI as a screening tool for prostate cancer: current evidence and future challenges. World J Urol. 2023 Apr;41(4):921–8. 10.1007/s00345-022-03947-y DOI: https://doi.org/10.1007/s00345-022-03947-y
  45. Crawford ED, Rosenberg MT, Partin AW, Cooperberg MR, Maccini M, Loeb S, et al. An Approach Using PSA Levels of 1.5 ng/mL as the Cutoff for Prostate Cancer Screening in Primary Care. Urology. 2016 Oct;96:116–20. 10.1016/j.urology.2016.07.001 DOI: https://doi.org/10.1016/j.urology.2016.07.001
  46. Lin K, Croswell J, Koenig H. Prostate-Specific Antigen-Based Screening for Prostate Cancer: An Evidence Update for the U.S. Preventive Services Task Force. Rockv Agency Healthc Res Qual (US); Evidence S.
  47. Grönberg H, Adolfsson J, Aly M, Nordström T, Wiklund P, Brandberg Y, et al. Prostate cancer screening in men aged 50-69 years (STHLM3): a prospective population-based diagnostic study. Lancet Oncol. 2015 Dec;16(16):1667–76. 10.1016/S1470-2045(15)00361-7 DOI: https://doi.org/10.1016/S1470-2045(15)00361-7
  48. Grönberg H, Eklund M, Picker W, Aly M, Jäderling F, Adolfsson J, et al. Prostate Cancer Diagnostics Using a Combination of the Stockholm3 Blood Test and Multiparametric Magnetic Resonance Imaging. Eur Urol. 2018 Dec;74(6):722–8. 10.1016/j.eururo.2018.06.022 DOI: https://doi.org/10.1016/j.eururo.2018.06.022
  49. Elyan A, Saba K, Sigle A, Wetterauer C, Engesser C, Püschel H, et al. Prospective Multicenter Validation of the Stockholm3 Test in a Central European Cohort. Eur Urol Focus. 2023 Oct;S2405-4569(23)00216-X. 10.1016/j.euf.2023.09.016 DOI: https://doi.org/10.1016/j.euf.2023.09.016
  50. Parekh DJ, Punnen S, Sjoberg DD, Asroff SW, Bailen JL, Cochran JS, 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 Sep;68(3):464–70. 10.1016/j.eururo.2014.10.021 DOI: https://doi.org/10.1016/j.eururo.2014.10.021
  51. Bryant RJ, Sjoberg DD, Vickers AJ, Robinson MC, Kumar R, Marsden L, 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. 2015 Apr;107(7):djv095. 10.1093/jnci/djv095 DOI: https://doi.org/10.1093/jnci/djv095
  52. Bhattu AS, Zappala SM, Parekh DJ, Punnen S. A 4Kscore Cut-off of 7.5% for Prostate Biopsy Decisions Provides High Sensitivity and Negative Predictive Value for Significant Prostate Cancer. Urology. 2021 Feb;148:53–8. 10.1016/j.urology.2020.11.008 DOI: https://doi.org/10.1016/j.urology.2020.11.008
  53. Auvinen A, Rannikko A, Taari K, Kujala P, Mirtti T, Kenttämies A, et al. A randomized trial of early detection of clinically significant prostate cancer (ProScreen): study design and rationale. Eur J Epidemiol. 2017 Jun;32(6):521–7. 10.1007/s10654-017-0292-5 DOI: https://doi.org/10.1007/s10654-017-0292-5
  54. Carlsson SV, Arnsrud Godtman R, Pihl CG, Vickers A, Lilja H, Hugosson J, et al. Young Age on Starting Prostate-specific Antigen Testing Is Associated with a Greater Reduction in Prostate Cancer Mortality: 24-Year Follow-up of the Göteborg Randomized Population-based Prostate Cancer Screening Trial [Erratum in: Eur Urol. 2022 Dec 8; PMID: 36334968; PMCID: PMC10481420]. Eur Urol. 2023 Feb;83(2):103–9. 10.1016/j.eururo.2022.10.006 DOI: https://doi.org/10.1016/j.eururo.2022.10.006
  55. Vickers AJ, Ulmert D, Sjoberg DD, Bennette CJ, Bjork T, Gerdtsson A, et al. Strategy for detection of prostate cancer based on relation between prostate specific antigen at age 40-55 and long term risk of metastasis: case-control study. BMJ . 2013 Apr 16;346(apr15 5):f2023–f2023. DOI: https://doi.org/10.1136/bmj.f2023
  56. Ventimiglia E, Bill-Axelson A, Bratt O, Montorsi F, Stattin P, Garmo H. Long-term Outcomes Among Men Undergoing Active Surveillance for Prostate Cancer in Sweden. JAMA Netw Open. 2022 Sep;5(9):e2231015. 10.1001/jamanetworkopen.2022.31015 DOI: https://doi.org/10.1001/jamanetworkopen.2022.31015
  57. Hamdy FC, Donovan JL, Lane JA, Metcalfe C, Davis M, Turner EL, et al.; ProtecT Study Group. Fifteen-Year Outcomes after Monitoring, Surgery, or Radiotherapy for Prostate Cancer. N Engl J Med. 2023 Apr;388(17):1547–58. 10.1056/NEJMoa2214122
  58. Willemse PM, Davis NF, Grivas N, Zattoni F, Lardas M, Briers E, et al. Systematic Review of Active Surveillance for Clinically Localised Prostate Cancer to Develop Recommendations Regarding Inclusion of Intermediate-risk Disease, Biopsy Characteristics at Inclusion and Monitoring, and Surveillance Repeat Biopsy Strategy. Eur Urol. 2022 Apr;81(4):337–46. 10.1016/j.eururo.2021.12.007 DOI: https://doi.org/10.1016/S0302-2838(22)01126-5
  59. Porter KK, King A, Galgano SJ, Sherrer RL, Gordetsky JB, Rais-Bahrami S. Financial implications of biparametric prostate MRI. Prostate Cancer Prostatic Dis. 2020 Mar;23(1):88–93. 10.1038/s41391-019-0158-x DOI: https://doi.org/10.1038/s41391-019-0158-x
  60. Winkel DJ, Wetterauer C, Matthias MO, Lou B, Shi B, Kamen A, et al. Autonomous Detection and Classification of PI-RADS Lesions in an MRI Screening Population Incorporating Multicenter-Labeled Deep Learning and Biparametric Imaging: Proof of Concept. Diagnostics (Basel, Switzerland) . 2020 Nov 14;10(11). DOI: https://doi.org/10.3390/diagnostics10110951
  61. Giganti F, Ng A, Asif A, Chan VW, Rossiter M, Nathan A, et al.; PRIME Quality Improvement Group. Global Variation in Magnetic Resonance Imaging Quality of the Prostate. Radiology. 2023 Oct;309(1):e231130. 10.1148/radiol.231130
  62. Giganti F, Allen C, Emberton M, Moore CM, Kasivisvanathan V; PRECISION study group. Prostate Imaging Quality (PI-QUAL): A New Quality Control Scoring System for Multiparametric Magnetic Resonance Imaging of the Prostate from the PRECISION trial. Eur Urol Oncol. 2020 Oct;3(5):615–9. 10.1016/j.euo.2020.06.007 DOI: https://doi.org/10.1016/j.euo.2020.06.007
  63. Saba K, Wettstein MS, Lieger L, Hötker AM, Donati OF, Moch H, et al. External Validation and Comparison of Prostate Cancer Risk Calculators Incorporating Multiparametric Magnetic Resonance Imaging for Prediction of Clinically Significant Prostate Cancer. J Urol. 2020 Apr;203(4):719–26. 10.1097/JU.0000000000000622 DOI: https://doi.org/10.1097/JU.0000000000000622
  64. SWOP Prostate Cancer Research Foundation Risk Calculator. https://www.prostatecancer-riskcalculator.com/
  65. Poyet C, Wettstein MS, Lundon DJ, Bhindi B, Kulkarni GS, Saba K, et al. External Evaluation of a Novel Prostate Cancer Risk Calculator (ProstateCheck) Based on Data from the Swiss Arm of the ERSPC. J Urol. 2016 Nov;196(5):1402–7. 10.1016/j.juro.2016.05.081 DOI: https://doi.org/10.1016/j.juro.2016.05.081
  66. Ong HT. β blockers in hypertension and cardiovascular disease. BMJ. 2007 May;334(7600):946–9. 10.1136/bmj.39185.440382.47 DOI: https://doi.org/10.1136/bmj.39185.440382.47
  67. Uhlig K, Balk EM, Earley A, Persson R, Garlitski AC, Chen M, Lamont JL, Miligkos M, Avendano EE. Assessment on Implantable Defibrillators and the Evidence for Primary Prevention of Sudden Cardiac Death [Internet]. Rockville (MD): Agency for Healthcare Research and Quality (US); 2013 Jun 26. PMID: 25356453.

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