Abstract
Ever since screening for early breast cancer (BC) diagnosis was shown to decrease mortality from the disease, screening programs have been widely implemented throughout the world. Targeted age groups and schedules vary between countries but the majority use a population-based approach, regardless of personal BC risk. The purpose of this review was to describe current population-based screening practices, point out some of the shortcomings of these practices, describe BC risk factors and risk assessment models, and present ongoing clinical trials of personalized risk-adapted BC screening. Three ongoing, large-scale, randomized controlled clinical trials (WISDOM in the US, MyPEBS in Europe, and TBST in Italy) were identified through a search of the MEDLINE and US National Library of Medicine (ClinicalTrials.gov) databases. In these trials, women either undergo standard or personalized screening. The trials vary in methods of risk stratification and screening modalities, but all aim to examine whether personalized risk-adapted screening can safely replace the current population-based approach and lead to rates of advanced-stage BC at diagnosis comparable with those of current screening regimens. The results of these trials may change current population-based screening practices.
References
Shapiro S, Venet W, Strax P et al. Ten- to fourteen-year effect of screening on breast cancer mortality. J Natl Cancer Inst. 1982;69:349–55.
Miller AB, Baines CJ, To T, Wall C. Canadian National Breast Screening Study: 1. Breast cancer detection and death rates among women aged 40 to 49 years. CMAJ .1992;147:1459–76.
Miller AB, Baines CJ, To T, Wall C. Canadian National Breast Screening Study: 2. Breast cancer detection and death rates among women aged 50–59 years. CMAJ. 1992;147:1477–88.
Andersson I, Janzon L. Reduced breast cancer mortality in women under age 50: updated results from the Malmo Mammographic Screening Program. J Natl Cancer Inst Monogr. 1997;(22):63–7.
Tabar L, Fagerberg CJ, Gad A, et al. Reduction in mortality from breast cancer after mass screening with mammography. Randomised trial from the Breast Cancer Screening Working Group of the Swedish National Board of Health and Welfare. Lancet. 1985;1:829–32.
Frisell J, Lidbrink E, Hellstrom L, Rutqvist LE. Followup after 11 years–update of mortality results in the Stockholm mammographic screening trial. Breast Cancer Res Treat. 1997;45:263–70.
Alexander FE, Anderson TJ, Brown HK, et al. The Edinburgh randomised trial of breast cancer screening: results after 10 years of follow-up. Br J Cancer. 1994;70:542–8.
Bjurstam N, Bjorneld L, Warwick J, et al. The Gothenburg Breast Screening Trial. Cancer. 2003;97:2387–96.
Humphrey LL, Helfand M, Chan BK, Woolf SH. Breast cancer screening: a summary of the evidence for the U.S. Preventive Services Task Force. Ann Intern Med. 2002;137:347–60.
Tabár L, Dean PB, Chen TH, et al. The incidence of fatal breast cancer measures the increased effectiveness of therapy in women participating in mammography screening. Cancer, 2019;125:515–23.
Ballard-Barbash R, Klabunde C, Paci E, et al. Breast cancer screening in 21 countries: delivery of services, notification of results and outcomes ascertainment. Eur J Cancer Prev. 1999;8:417–26.
Altobelli E, Lattanzi A. Breast cancer in European Union: an update of screening programmes as of March 2014 (review). Int J Oncol. 2014;45:1785–92.
Bevers TB, Anderson BO, Bonaccio E, et al. NCCN clinical practice guidelines in oncology: breast cancer screening and diagnosis. J Natl Compr Canc Netw. 2009;7:1060–96.
Siu AL. Screening for Breast Cancer: U.S. Preventive Services Task Force Recommendation Statement. Ann Intern Med. 2016;164:279–96.
Gradishar WJ, Anderson BO, Abraham J, et al. Breast Cancer, Version 3.2020, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw. 2020;18:452–78.
Lee CS, Bhargavan-Chatfield M, Burnside ES et al. The National Mammography Database: Preliminary Data. AJR Am J Roentgenol. 2016;206:883–90.
Gur D, Sumkin JH, Hardesty LA, et al. Recall and detection rates in screening mammography. Cancer. 2004;100:1590–94.
Elmore JG, Barton MB, Moceri VM, et al. Ten-year risk of false positive screening mammograms and clinical breast examinations. N Engl J Med. 1998;338:1089–96.
Hofvind S, Ponti A, Patnick J, et al. False-positive results in mammographic screening for breast cancer in Europe: a literature review and survey of service screening programmes. J Med Screen. 2012;19 Suppl 1:57–66.
Hubbard RA, Kerlikowske K, Flowers CI, et al. Cumulative probability of false-positive recall or biopsy recommendation after 10 years of screening mammography: a cohort study. Ann Intern Med. 2011;155:481–92.
Johns LE, Moss SM. False-positive results in the randomized controlled trial of mammographic screening from age 40 (“Age” trial). Cancer Epidemiol Biomarkers Prev. 2010;19:2758–64.
Roman M, Skaane P, Hofvind S. The cumulative risk of false-positive screening results across screening centres in the Norwegian Breast Cancer Screening Program. Eur J Radiol. 2014;83:1639–44.
Singh D, Pitkaniemi J, Malila N, Anttila A. Cumulative risk of false positive test in relation to breast symptoms in mammography screening: a historical prospective cohort study. Breast Cancer Res Treat. 2016;159:305–13.
Dabbous FM, Dolecek TA, Berbaum ML, et al. Impact of a False-Positive Screening Mammogram on Subsequent Screening Behavior and Stage at Breast Cancer Diagnosis. Cancer Epidemiol Biomarkers Prev. 2017;26:397–403.
Román R, Sala M, De La Vega M, et al. Effect of false-positives and women’s characteristics on long-term adherence to breast cancer screening. Breast Cancer Res Treat. 2011;130:543–52.
Bare M, Tora N, Salas D, et al. Mammographic and clinical characteristics of different phenotypes of screen-detected and interval breast cancers in a nationwide screening program. Breast Cancer Res Treat. 2015;154:403–15.
Blanch J, Sala M, Ibanez J, et al. Impact of risk factors on different interval cancer subtypes in a population-based breast cancer screening programme. PLoS One. 2014;9:e110207.
Domingo L, Salas D, Zubizarreta R, et al. Tumor phenotype and breast density in distinct categories of interval cancer: results of population-based mammography screening in Spain. Breast Cancer Res. 2014;16:R3.
Holm J, Humphreys K, Li J, et al. Risk factors and tumor characteristics of interval cancers by mammographic density. J Clin Oncol. 2015;33:1030–7.
Mandelson MT, Oestreicher N, Porter PL, et al. Breast density as a predictor of mammographic detection: comparison of interval- and screen-detected cancers. J Natl Cancer Inst. 2000;92:1081–7.
Porter PL, El-Bastawissi AY, Mandelson MT, et al. Breast tumor characteristics as predictors of mammographic detection: comparison of interval- and screen-detected cancers. J Natl Cancer Inst. 1999;91:2020–8.
Roubidoux MA, Bailey JE, Wray LA, Helvie MA. Invasive cancers detected after breast cancer screening yielded a negative result: relationship of mammographic density to tumor prognostic factors. Radiology. 2004;230:42–8.
Rebolj M, Assi V, Brentnall A, et al. Addition of ultrasound to mammography in the case of dense breast tissue: systematic review and meta-analysis. Br J Cancer. 2018;118:1559–70.
Kuhl CK. Abbreviated breast MRI for screening women with dense breast: the EA1141 trial. Br J Radiol. 2018;91:20170441.
Bakker MF, de Lange SV, Pijnappel RM, et al. Supplemental MRI Screening for Women with Extremely Dense Breast Tissue. N Engl J Med. 2019;381:2091–102.
Kalager M, Adami HO, Bretthauer M, Tamimi RM. Overdiagnosis of invasive breast cancer due to mammography screening: results from the Norwegian screening program. Ann Intern Med. 2012;156:491–9.
Falk RS, Hofvind S, Skaane P, Haldorsen T. Overdiagnosis among women attending a population-based mammography screening program. Int J Cancer. 2013;133:705–12.
Loberg M, Lousdal ML, Bretthauer M, Kalager M. Benefits and harms of mammography screening. Breast Cancer Res. 2015;17:63.
Webb ML, Cady B, Michaelson JS, et al. A failure analysis of invasive breast cancer: most deaths from disease occur in women not regularly screened. Cancer. 2014;120:2839–46.
Menarche, menopause, and breast cancer risk: individual participant meta-analysis, including 118 964 women with breast cancer from 117 epidemiological studies. Lancet Oncol. 2012;13:1141–51.
Easton DF. Familial risks of breast cancer. Breast Cancer Res. 2002;4:179.
Ma H, Bernstein L, Pike MC, Ursin G. Reproductive factors and breast cancer risk according to joint estrogen and progesterone receptor status: a meta-analysis of epidemiological studies. Breast Cancer Res. 2006;8:R43.
Lahmann PH, Hoffmann K, Allen N, et al. Body size and breast cancer risk: findings from the European Prospective Investigation into Cancer And Nutrition (EPIC). Int J Cancer. 2004;111:762–71.
Dyrstad SW, Yan Y, Fowler AM, Colditz GA. Breast cancer risk associated with benign breast disease: systematic review and meta-analysis. Breast Cancer Res Treat. 2015;149:569–75.
Menes TS, Kerlikowske K, Lange J, et al. Subsequent Breast Cancer Risk Following Diagnosis of Atypical Ductal Hyperplasia on Needle Biopsy. JAMA Oncol. 2017;3:36–41.
Travis LB, Hill D, Dores GM, et al. Cumulative absolute breast cancer risk for young women treated for Hodgkin lymphoma. J Natl Cancer Inst. 2005;97:1428–37.
Type and timing of menopausal hormone therapy and breast cancer risk: individual participant meta-analysis of the worldwide epidemiological evidence. Lancet. 2019;394:1159–68.
Boyd NF, Rommens JM, Vogt K, et al. Mammographic breast density as an intermediate phenotype for breast cancer. Lancet Oncol. 2005;6:798–808.
Boyd NF, Guo H, Martin LJ, et al. Mammographic density and the risk and detection of breast cancer. N Engl J Med. 2007;356:227–36.
McCormack VA, dos Santos Silva I. Breast density and parenchymal patterns as markers of breast cancer risk: a meta-analysis. Cancer Epidemiol Biomarkers Prev. 2006;15:1159–69.
Saslow D, Boetes C, Burke W, et al. American Cancer Society guidelines for breast screening with MRI as an adjunct to mammography. CA Cancer J Clin. 2007;57:75–89.
Gail MH, Brinton LA, Byar DP, et al. Projecting individualized probabilities of developing breast cancer for white females who are being examined annually. J Natl Cancer Inst. 1989;81:1879–86.
Claus EB, Risch N, Thompson WD. Autosomal dominant inheritance of early-onset breast cancer. Implications for risk prediction. Cancer. 1994;73:643–51.
Tyrer J, Duffy SW, Cuzick J. A breast cancer prediction model incorporating familial and personal risk factors. Stat Med. 2004;23:1111–30.
Lee A, Mavaddat N, Wilcox AN, et al. BOADICEA: a comprehensive breast cancer risk prediction model incorporating genetic and nongenetic risk factors. Genet Med. 2019;21:1708–18.
Chen S, Wang W, Broman KW, et al. BayesMendel: an R environment for Mendelian risk prediction. Stat Appl Genet Mol Biol. 2004;3:Article21.
Brentnall AR, Harkness EF, Astley SM, et al. Mammographic density adds accuracy to both the Tyrer-Cuzick and Gail breast cancer risk models in a prospective UK screening cohort. Breast Cancer Res. 2015;17:147.
Mavaddat N, Antoniou AC, Easton DF, Garcia-Closas M. Genetic susceptibility to breast cancer. Mol Oncol. 2010;4:174–91.
Easton DF, Pooley KA, Dunning AM, et al. Genome-wide association study identifies novel breast cancer susceptibility loci. Nature. 2007;447:1087–93.
Michailidou K, Hall P, Gonzalez-Neira A, et al. Large-scale genotyping identifies 41 new loci associated with breast cancer risk. Nat Genet. 2013;45:353–61, 361e1–2.
Mavaddat N, Michailidou K, Dennis J, et al. Polygenic Risk Scores for Prediction of Breast Cancer and Breast Cancer Subtypes. Am J Hum Genet. 2019;104:21–34.
Mavaddat N, Pharoah PD, Michailidou K, et al. Prediction of breast cancer risk based on profiling with common genetic variants. J Natl Cancer Inst. 2015;107:djv036.
Yala A, Lehman C, Schuster T, et al. A Deep Learning Mammography-based Model for Improved Breast Cancer Risk Prediction. Radiology. 2019;292:60–6.
Yuan WH, Hsu HC, Chen YY, Wu CH. Supplemental breast cancer-screening ultrasonography in women with dense breasts: a systematic review and meta-analysis. Br J Cancer. 2020;123:673–88.
Weinstein SP, Korhonen K, Cirelli C, et al. Abbreviated Breast Magnetic Resonance Imaging for Supplemental Screening of Women With Dense Breasts and Average Risk. J Clin Oncol. 2020;38:3874–82.
Paci E, Mantellini P, Giorgi Rossi P, et al. Tailored Breast Screening Trial (TBST) [in Italian]. Epidemiol Prev. 2013;37:317–27.
Shieh Y, Eklund M, Madlensky L, et al. Breast Cancer Screening in the Precision Medicine Era: Risk-Based Screening in a Population-Based Trial. J Natl Cancer Inst. 2017;109(5).
Esserman LJ. The WISDOM Study: breaking the deadlock in the breast cancer screening debate. NPJ Breast Cancer. 2017;3:34.
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Tanir M. Allweis, Naama Hermann, Rinat Berenstein-Molho, and Michal Guindy report no conflicts of interest.
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Allweis, T.M., Hermann, N., Berenstein-Molho, R. et al. Personalized Screening for Breast Cancer: Rationale, Present Practices, and Future Directions. Ann Surg Oncol 28, 4306–4317 (2021). https://doi.org/10.1245/s10434-020-09426-1
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DOI: https://doi.org/10.1245/s10434-020-09426-1