Benefits and harms of annual, biennial, or triennial breast cancer mammography screening for women at average risk of breast cancer: a systematic review for the European Commission Initiative on Breast Cancer (ECIBC).
Journal
British journal of cancer
ISSN: 1532-1827
Titre abrégé: Br J Cancer
Pays: England
ID NLM: 0370635
Informations de publication
Date de publication:
03 2022
03 2022
Historique:
received:
09
10
2020
accepted:
30
07
2021
revised:
20
06
2021
pubmed:
28
11
2021
medline:
11
3
2022
entrez:
27
11
2021
Statut:
ppublish
Résumé
Although mammography screening is recommended in most European countries, the balance between the benefits and harms of different screening intervals is still a matter of debate. This review informed the European Commission Initiative on Breast Cancer (BC) recommendations. We searched PubMed, EMBASE, and the Cochrane Library to identify RCTs, observational or modelling studies, comparing desirable (BC deaths averted, QALYs, BC stage, interval cancer) and undesirable (overdiagnosis, false positive related, radiation related) effects from annual, biennial, or triennial mammography screening in women of average risk for BC. We assessed the certainty of the evidence using the GRADE approach. We included one RCT, 13 observational, and 11 modelling studies. In women 50-69, annual compared to biennial screening may have small additional benefits but an important increase in false positive results; triennial compared to biennial screening may have smaller benefits while avoiding some harms. In younger women (aged 45-49), annual compared to biennial screening had a smaller gain in benefits and larger harms, showing a less favourable balance in this age group than in women 50-69. In women 70-74, there were fewer additional harms and similar benefits with shorter screening intervals. The overall certainty of the evidence for each of these comparisons was very low. In women of average BC risk, screening intervals have different trade-offs for each age group. The balance probably favours biennial screening in women 50-69. In younger women, annual screening may have a less favourable balance, while in women aged 70-74 years longer screening intervals may be more favourable.
Sections du résumé
BACKGROUND
Although mammography screening is recommended in most European countries, the balance between the benefits and harms of different screening intervals is still a matter of debate. This review informed the European Commission Initiative on Breast Cancer (BC) recommendations.
METHODS
We searched PubMed, EMBASE, and the Cochrane Library to identify RCTs, observational or modelling studies, comparing desirable (BC deaths averted, QALYs, BC stage, interval cancer) and undesirable (overdiagnosis, false positive related, radiation related) effects from annual, biennial, or triennial mammography screening in women of average risk for BC. We assessed the certainty of the evidence using the GRADE approach.
RESULTS
We included one RCT, 13 observational, and 11 modelling studies. In women 50-69, annual compared to biennial screening may have small additional benefits but an important increase in false positive results; triennial compared to biennial screening may have smaller benefits while avoiding some harms. In younger women (aged 45-49), annual compared to biennial screening had a smaller gain in benefits and larger harms, showing a less favourable balance in this age group than in women 50-69. In women 70-74, there were fewer additional harms and similar benefits with shorter screening intervals. The overall certainty of the evidence for each of these comparisons was very low.
CONCLUSIONS
In women of average BC risk, screening intervals have different trade-offs for each age group. The balance probably favours biennial screening in women 50-69. In younger women, annual screening may have a less favourable balance, while in women aged 70-74 years longer screening intervals may be more favourable.
Identifiants
pubmed: 34837076
doi: 10.1038/s41416-021-01521-8
pii: 10.1038/s41416-021-01521-8
pmc: PMC8854566
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Systematic Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
673-688Informations de copyright
© 2021. Springer.
Références
Ferlay J, Ervik M, Lam F, Colombet M, Mery L, Piñeros M et al. Global Cancer Observatory: Cancer Today. Lyon, France: International Agency for Research on Cancer. Available from: https://gco.iarc.fr/today , accessed [25-07-2019]. 2018.
ECIS. European Cancer Information System From https://ecis.jrc.ec.europa.eu , accessed on 20-July-2019. 2018.
Duffy SW, Tabar L, Yen AM, Dean PB, Smith RA, Jonsson H, et al. Mammography screening reduces rates of advanced and fatal breast cancers: Results in 549,091 women. Cancer. 2020;126:2971–9.
pubmed: 32390151
doi: 10.1002/cncr.32859
Borrelli C, Cohen S., Duncan A, Given-Wilson R, Jenkins J, Kearins O, et al. NHS Breast Screening Programme. Clinical guidance for breast cancer screening assessment. Fourth edition Nov 2016.
Siu AL, Force, U. S. P. S. T. Screening for breast cancer: U.S. Preventive services task force recommendation statement. Ann Intern Med. 2016;164:279–96.
pubmed: 26757170
doi: 10.7326/M15-2886
Oeffinger KC, Fontham ET, Etzioni R, Herzig A, Michaelson JS, Shih YC, et al. Breast cancer screening for women at average risk: 2015 guideline update from the American Cancer Society. JAMA. 2015;314:1599–614.
pubmed: 26501536
pmcid: 4831582
doi: 10.1001/jama.2015.12783
Mandelblatt JS, Stout NK, Schechter CB, van den Broek JJ, Miglioretti DL, Krapcho M, et al. Collaborative modeling of the benefits and harms associated with different U.S. Breast Cancer Screening Strategies. Ann Intern Med. 2016;164:215–25.
pubmed: 26756606
pmcid: 5079106
doi: 10.7326/M15-1536
Kerlikowske K, Zhu W, Hubbard RA, Geller B, Dittus K, Braithwaite D, et al. Outcomes of screening mammography by frequency, breast density, and postmenopausal hormone therapy. JAMA Intern Med. 2013;173:807–16.
pubmed: 23552817
pmcid: 3699693
doi: 10.1001/jamainternmed.2013.307
Schunemann HJ, Lerda D, Dimitrova N, Alonso-Coello P, Grawingholt A, Quinn C, et al. Methods for development of the European Commission Initiative on Breast Cancer Guidelines: recommendations in the era of guideline transparency. Ann Intern Med. 2019;171:273–80.
pubmed: 31330534
doi: 10.7326/M18-3445
Schunemann HJ, Lerda D, Quinn C, Follmann M, Alonso-Coello P, Rossi PG, et al. Breast cancer screening and diagnosis: a synopsis of the European Breast Guidelines. Ann Intern Med. 2019;172:46–56.
pubmed: 31766052
doi: 10.7326/M19-2125
Guyatt GH, Oxman AD, Kunz R, Atkins D, Brozek J, Vist G. et al. GRADE guidelines: 2. Framing the question and deciding on important outcomes. J Clin Epidemiol.2011;64:395–400.
pubmed: 21194891
doi: 10.1016/j.jclinepi.2010.09.012
Higgins JP, Altman DG, Gotzsche PC, Juni P, Moher D, Oxman AD, et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ. 2011;343:d5928.
pubmed: 22008217
pmcid: 3196245
doi: 10.1136/bmj.d5928
Sterne JA, Hernan MA, Reeves BC, Savovic J, Berkman ND, Viswanathan M, et al. ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ. 2016;355:i4919.
pubmed: 27733354
pmcid: 5062054
doi: 10.1136/bmj.i4919
Jaime Caro J, Eddy DM, Kan H, Kaltz C, Patel B, Eldessouki R, et al. Questionnaire to assess relevance and credibility of modeling studies for informing health care decision making: an ISPOR-AMCP-NPC Good Practice Task Force report. Value Health. 2014;17:174–82.
pubmed: 24636375
doi: 10.1016/j.jval.2014.01.003
Guyatt GH, Oxman AD, Schunemann HJ, Tugwell P, Knottnerus A. GRADE guidelines: a new series of articles in the Journal of Clinical Epidemiology. J Clin. Epidemiol. 2011;64:380–2.
pubmed: 21185693
doi: 10.1016/j.jclinepi.2010.09.011
Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 2008;336:924–6.
pubmed: 18436948
pmcid: 2335261
doi: 10.1136/bmj.39489.470347.AD
Hultcrantz M, Rind D, Akl EA, Treweek S, Mustafa RA, Iorio A, et al. The GRADE Working Group clarifies the construct of certainty of evidence. J Clin Epidemio. 2017;87:4–13.
doi: 10.1016/j.jclinepi.2017.05.006
Duffy SW, B. R. Long term mortality results from the UK screening frequency trial. EJC Supplements. 2008;6:48.
doi: 10.1016/S1359-6349(08)70316-1
Breast Screening Frequency Trial, G. The frequency of breast cancer screening: results from the UKCCCR Randomised Trial. United Kingdom Co-ordinating Committee on Cancer Research. Eur J Cancer. 2002;38:1458–64.
doi: 10.1016/S0959-8049(01)00397-5
Gunsoy NB, Garcia-Closas M, Moss SM. Estimating breast cancer mortality reduction and overdiagnosis due to screening for different strategies in the United Kingdom. Br J Cancer. 2014;110:2412–9.
pubmed: 24762956
pmcid: 4021535
doi: 10.1038/bjc.2014.206
Miglioretti DL, Lange J, van den Broek JJ, Lee CI, van Ravesteyn NT, Ritley D, et al. Radiation-induced breast cancer incidence and mortality from digital mammography screening: a modeling study. Ann Intern Med. 2016;164:205–14.
pubmed: 26756460
pmcid: 4878445
doi: 10.7326/M15-1241
Trentham-Dietz A, Kerlikowske K, Stout NK, Miglioretti DL, Schechter CB, Ergun MA, et al. Tailoring Breast Cancer Screening Intervals by Breast Density and Risk for Women Aged 50 Years or Older: Collaborative Modeling of Screening Outcomes. Ann intern Med. 2016;165:700–12.
pubmed: 27548583
pmcid: 5125086
doi: 10.7326/M16-0476
Tsunematsu M, Kakehashi M. An analysis of mass screening strategies using a mathematical model: comparison of breast cancer screening in Japan and the United States. J Epidemiol. 2015;25:162–71.
pubmed: 25483105
doi: 10.2188/jea.JE20140047
van Ravesteyn NT, Miglioretti DL, Stout NK, Lee SJ, Schechter CB, Buist DS, et al. Tipping the balance of benefits and harms to favor screening mammography starting at age 40 years: a comparative modeling study of risk. Ann Intern Med. 2012;156:609–17.
pubmed: 22547470
pmcid: 3520058
doi: 10.7326/0003-4819-156-9-201205010-00002
Yaffe MJ, Mainprize JG. Risk of radiation-induced breast cancer from mammographic screening. Radiology. 2011;258:98–105.
pubmed: 21081671
doi: 10.1148/radiol.10100655
Yaffe MJ, Mittmann N, Lee P, Tosteson AN, Trentham-Dietz A, Alagoz O, et al. Clinical outcomes of modelling mammography screening strategies. Health Rep. 2015;26:9–15.
pubmed: 26676234
pmcid: 4869692
Vilaprinyo E, Forne C, Carles M, Sala M, Pla R, Castells X, et al. Cost-effectiveness and harm-benefit analyses of risk-based screening strategies for breast cancer. PLoS One. 2014;9:e86858.
pubmed: 24498285
pmcid: 3911927
doi: 10.1371/journal.pone.0086858
Mittmann N, Stout NK, Tosteson ANA, Trentham-Dietz A, Alagoz O, Yaffe MJ. Cost-effectiveness of mammography from a publicly funded health care system perspective. CMAJ Open. 2018;6:E77–E86.
pubmed: 29440151
pmcid: 5878949
doi: 10.9778/cmajo.20170106
Arnold M, Pfeifer K, Quante AS. Is risk-stratified breast cancer screening economically efficient in Germany? PLoS ONE. 2019;14:e0217213.
pubmed: 31120970
pmcid: 6532918
doi: 10.1371/journal.pone.0217213
Braithwaite D, Zhu W, Hubbard RA, O’Meara ES, Miglioretti DL, Geller B, et al. Screening outcomes in older US women undergoing multiple mammograms in community practice: does interval, age, or comorbidity score affect tumor characteristics or false positive rates? J Natl Cancer Inst. 2013;105:334–41.
pubmed: 23385442
pmcid: 3589257
doi: 10.1093/jnci/djs645
Coldman AJ, Phillips N, Olivotto IA, Gordon P, Warren L, Kan L. Impact of changing from annual to biennial mammographic screening on breast cancer outcomes in women aged 50-79 in British Columbia. J Med Scree. 2008;15:182–7.
doi: 10.1258/jms.2008.008064
Dittus K, Geller B, Weaver DL, Kerlikowske K, Zhu W, Hubbard R, et al. Impact of mammography screening interval on breast cancer diagnosis by menopausal status and BMI. J Gen Intern Med. 2013;28:1454–62.
pubmed: 23760741
pmcid: 3797353
doi: 10.1007/s11606-013-2507-0
Goel A, Littenberg B, Burack RC. The association between the pre-diagnosis mammography screening interval and advanced breast cancer. Breast Cancer Res Treat. 2007;102:339–45.
pubmed: 16927175
doi: 10.1007/s10549-006-9334-5
Hubbard RA, Kerlikowske K, Flowers CI, Yankaskas BC, Zhu W, Miglioretti DL. 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.
pubmed: 22007042
pmcid: 3209800
doi: 10.7326/0003-4819-155-8-201110180-00004
Hunt KA, Rosen EL, Sickles EA. Outcome analysis for women undergoing annual versus biennial screening mammography: a review of 24,211 examinations. AJR Am J Roentgenol. 1999;173:285–9.
pubmed: 10430120
doi: 10.2214/ajr.173.2.10430120
Klemi PJ, Toikkanen S, Rasanen O, Parvinen I, Joensuu H. Mammography screening interval and the frequency of interval cancers in a population-based screening. Br J Cancer. 1997;75:762–6.
pubmed: 9043038
pmcid: 2063348
doi: 10.1038/bjc.1997.135
Miglioretti DL, Zhu W, Kerlikowske K, Sprague BL, Onega T, Buist DS, et al. Breast tumor prognostic characteristics and biennial vs annual mammography, age, and menopausal status. JAMA Oncol. 2015;1:1069–77.
pubmed: 26501844
pmcid: 4644100
doi: 10.1001/jamaoncol.2015.3084
O’Meara ES, Zhu W, Hubbard RA, Braithwaite D, Kerlikowske K, Dittus KL, et al. Mammographic screening interval in relation to tumor characteristics and false-positive risk by race/ethnicity and age. Cancer. 2013;119:3959–67.
pubmed: 24037812
doi: 10.1002/cncr.28310
Parvinen I, Chiu S, Pylkkanen L, Klemi P, Immonen-Raiha P, Kauhava L, et al. Effects of annual vs triennial mammography interval on breast cancer incidence and mortality in ages 40-49 in Finland. Br J Cancer. 2011;105:1388–91.
pubmed: 21934688
pmcid: 3241549
doi: 10.1038/bjc.2011.372
White E, Miglioretti DL, Yankaskas BC, Geller BM, Rosenberg RD, Kerlikowske K, et al. Biennial versus annual mammography and the risk of late-stage breast cancer. J Natl Cancer Inst. 2004;96:1832–9.
pubmed: 15601639
doi: 10.1093/jnci/djh337
Sanderson M, Levine RS, Fadden MK, Kilbourne B, Pisu M, Cain V, et al. Mammography screening among the elderly: a research challenge. Am J Med. 2015;128:1362 e1367–1314.
doi: 10.1016/j.amjmed.2015.06.032
McGuinness JE, Ueng W, Trivedi MS, Yi HS, David R, Vanegas A, et al. Factors associated with false positive results on screening mammography in a population of predominantly Hispanic women. Cancer Epidemiol Biomarkers Prev. 2018;27:446–53.
pubmed: 29382701
pmcid: 5884721
doi: 10.1158/1055-9965.EPI-17-0009
Hubbard RA, Miglioretti DL, Smith RA. Modelling the cumulative risk of a false-positive screening test. Stat Methods Med Res. 2010;19:429–49.
pubmed: 20356857
pmcid: 2916076
doi: 10.1177/0962280209359842
Lee SJ, Li X, Huang H, Zelen M. The Dana-Farber CISNET model for breast cancer screening strategies: an update. Med Decis Making. 2018;38:44S–53S.
pubmed: 29554465
pmcid: 5929104
doi: 10.1177/0272989X17741634
van den Broek JJ, van Ravesteyn NT, Heijnsdijk EA, de Koning HJ. Simulating the Impact of Risk-Based Screening and Treatment on Breast Cancer Outcomes with MISCAN-Fadia. Med Decis Making. 2018;38:54S–65S.
pubmed: 29554469
pmcid: 5862065
doi: 10.1177/0272989X17711928
Schechter CB, Near AM, Jayasekera J, Chandler Y, Mandelblatt JS. Structure, function, and applications of the Georgetown-Einstein (GE) Breast Cancer Simulation Model. Med Decis Making. 2018;38:66S–77S.
pubmed: 29554462
pmcid: 5862062
doi: 10.1177/0272989X17698685
Huang X, Li Y, Song J, Berry DA. A Bayesian Simulation Model for Breast Cancer Screening, Incidence, Treatment, and Mortality. Med Decis Making. 2018 Apr;38(1_suppl):78S–88S.
Plevritis SK, Sigal BM, Salzman P, Rosenberg J, Glynn P. A stochastic simulation model of U.S. breast cancer mortality trends from 1975 to 2000. J Natl Cancer Inst Monogr. 2006; 86–95, https://doi.org/10.1093/jncimonographs/lgj012 .
Alagoz O, Ergun MA, Cevik M, Sprague BL, Fryback DG, Gangnon RE, et al. The University of Wisconsin breast cancer epidemiology simulation Model: an update. Med Decis Making. 2018;38:99S–111S.
pubmed: 29554470
pmcid: 5862066
doi: 10.1177/0272989X17711927
Mandelblatt JS, Near AM, Miglioretti DL, Munoz D, Sprague BL, Trentham-Dietz A, et al. Common model inputs used in CISNET collaborative breast cancer modeling. Med Decis Making. 2018;38:9S–23S.
pubmed: 29554466
pmcid: 5862072
doi: 10.1177/0272989X17700624
van den Broek JJ, van Ravesteyn NT, Mandelblatt JS, Cevik M, Schechter CB, Lee SJ, et al. Comparing CISNET breast cancer models using the maximum clinical incidence reduction methodology. Med Decis Making. 2018;38:112S–125S.
pubmed: 29554471
pmcid: 5862068
doi: 10.1177/0272989X17743244
Carles M, Vilaprinyo E, Cots F, Gregori A, Pla R, Roman R, et al. Cost-effectiveness of early detection of breast cancer in Catalonia (Spain). BMC Cancer. 2011;11:192.
pubmed: 21605383
pmcid: 3125279
doi: 10.1186/1471-2407-11-192
Lehman CD, Arao RF, Sprague BL, Lee JM, Buist DS, Kerlikowske K, et al. National performance benchmarks for modern screening digital mammography: update from the breast cancer surveillance consortium. Radiology. 2017;283:49–58.
pubmed: 27918707
doi: 10.1148/radiol.2016161174
Early Breast Cancer Trialists’ Collaborative, G, Peto R, Davies C, Godwin J, Gray R, Pan HC, et al. Comparisons between different polychemotherapy regimens for early breast cancer: meta-analyses of long-term outcome among 100,000 women in 123 randomised trials. Lancet. 2012;379:432–44.
doi: 10.1016/S0140-6736(11)61625-5
Myers ER, Moorman P, Gierisch JM, Havrilesky LJ, Grimm LJ, Ghate S, et al. Benefits and harms of breast cancer screening: a systematic review. JAMA. 2015;314:1615–34.
Ripping TM, Ten Haaf K, Verbeek ALM, van Ravesteyn NT & Broeders MJM. Quantifying overdiagnosis in cancer screening: a systematic review to evaluate the methodology. J Natl Cancer Inst. 2017;109:djx060.
Canelo-Aybar C, Ferreira DS, Ballesteros M, Posso M, Montero N, Sola I et al. Benefits and harms of breast cancer mammography screening for women at average risk of breast cancer: a systematic review for the European Commission Initiative on Breast Cancer. J. Med Screen. 2021; https://doi.org/10.1177/0969141321993866 .
Moss SM, Wale C, Smith R, Evans A, Cuckle H, Duffy SW. Effect of mammographic screening from age 40 years on breast cancer mortality in the UK Age trial at 17 years’ follow-up: a randomised controlled trial. Lancet. Oncol. 2015;16:1123–32.
pubmed: 26206144
doi: 10.1016/S1470-2045(15)00128-X
Sankatsing VD, Heijnsdijk EA, van Luijt PA, van Ravesteyn NT, Fracheboud J, de Koning HJ. Cost-effectiveness of digital mammography screening before the age of 50 in The Netherlands. Int J Cancer. 2015;137:1990–9.
pubmed: 25895135
doi: 10.1002/ijc.29572
Habbema JD, Wilt TJ, Etzioni R, Nelson HD, Schechter CB, Lawrence WF, et al. Models in the development of clinical practice guidelines. Ann Intern Med. 2014;161:812–8.
pubmed: 25437409
doi: 10.7326/M14-0845
Narayan AK, Elkin EB, Lehman CD, Morris EA. Quantifying performance thresholds for recommending screening mammography: a revealed preference analysis of USPSTF guidelines. Breast Cancer Res Treatment. 2018;172:463–8.
doi: 10.1007/s10549-018-4917-5
Hayward JH, Ray KM, Wisner DJ, Kornak J, Lin W, Joe BN, et al. Improving screening mammography outcomes through comparison with multiple prior mammograms. AJR Am J Roentgenol. 2016;207:918–24.
pubmed: 27385404
pmcid: 5654684
doi: 10.2214/AJR.15.15917
Roelofs AA, Karssemeijer N, Wedekind N, Beck C, van Woudenberg S, Snoeren PR, et al. Importance of comparison of current and prior mammograms in breast cancer screening. Radiology. 2007;242:70–77.
pubmed: 17185661
doi: 10.1148/radiol.2421050684
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.
pubmed: 16775176
doi: 10.1158/1055-9965.EPI-06-0034
Boyd NF, Guo H, Martin LJ, Sun L, Stone J, Fishell E, et al. Mammographic density and the risk and detection of breast cancer. N Engl J Med. 2007;356:227–36.
pubmed: 17229950
doi: 10.1056/NEJMoa062790