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1.
US Preventive Services Task Force.  Screening for breast cancer: US Preventive Services Task Force recommendation statement.  Ann Intern Med. 2009;151(10):716-726, W-236.PubMedGoogle ScholarCrossref
2.
Mandelblatt  JS, Cronin  KA, Bailey  S,  et al; Breast Cancer Working Group of the Cancer Intervention and Surveillance Modeling Network.  Effects of mammography screening under different screening schedules: model estimates of potential benefits and harms.  Ann Intern Med. 2009;151(10):738-747.PubMedGoogle ScholarCrossref
3.
Smith  RA, Brooks  D, Cokkinides  V, Saslow  D, Brawley  OW.  Cancer screening in the United States, 2013: a review of current American Cancer Society guidelines, current issues in cancer screening, and new guidance on cervical cancer screening and lung cancer screening.  CA Cancer J Clin. 2013;63(2):88-105.PubMedGoogle ScholarCrossref
4.
American College of Obstetricians-Gynecologists.  Practice Bulletin No. 122: breast cancer screening.  Obstet Gynecol. 2011;118(2, pt 1):372-382.PubMedGoogle ScholarCrossref
5.
Bevers  TB, Anderson  BO, Bonaccio  E,  et al; National Comprehensive Cancer Network.  NCCN clinical practice guidelines in oncology: breast cancer screening and diagnosis.  J Natl Compr Canc Netw. 2009;7(10):1060-1096.PubMedGoogle Scholar
6.
Lee  CH, Dershaw  DD, Kopans  D,  et al.  Breast cancer screening with imaging: recommendations from the Society of Breast Imaging and the ACR on the use of mammography, breast MRI, breast ultrasound, and other technologies for the detection of clinically occult breast cancer.  J Am Coll Radiol. 2010;7(1):18-27.PubMedGoogle ScholarCrossref
7.
Ichikawa  LE, Barlow  WE, Anderson  ML, Taplin  SH, Geller  BM, Brenner  RJ; National Cancer Institute-sponsored Breast Cancer Surveillance Consortium.  Time trends in radiologists’ interpretive performance at screening mammography from the community-based Breast Cancer Surveillance Consortium, 1996-2004.  Radiology. 2010;256(1):74-82.PubMedGoogle ScholarCrossref
8.
Kerlikowske  K, Hubbard  RA, Miglioretti  DL,  et al; Breast Cancer Surveillance Consortium.  Comparative effectiveness of digital versus film-screen mammography in community practice in the United States: a cohort study.  Ann Intern Med. 2011;155(8):493-502.PubMedGoogle ScholarCrossref
9.
Brawley  OW.  Risk-based mammography screening: an effort to maximize the benefits and minimize the harms.  Ann Intern Med. 2012;156(9):662-663.PubMedGoogle ScholarCrossref
10.
Vilaprinyo  E, Forné  C, Carles  M,  et al; Interval Cancer (INCA) Study Group.  Cost-effectiveness and harm-benefit analyses of risk-based screening strategies for breast cancer.  PLoS One. 2014;9(2):e86858.PubMedGoogle ScholarCrossref
11.
Mandelblatt  JS, Stout  N, Trentham-Dietz  A.  To screen or not to screen women in their 40s for breast cancer: is personalized risk-based screening the answer?  Ann Intern Med. 2011;155(1):58-60.PubMedGoogle ScholarCrossref
12.
Onega  T, Beaber  EF, Sprague  BL,  et al.  Breast cancer screening in an era of personalized regimens: a conceptual model and National Cancer Institute initiative for risk-based and preference-based approaches at a population level.  Cancer. 2014;120(19):2955-2964.PubMedGoogle ScholarCrossref
13.
Schousboe  JT, Kerlikowske  K, Loh  A, Cummings  SR.  Personalizing mammography by breast density and other risk factors for breast cancer: analysis of health benefits and cost-effectiveness.  Ann Intern Med. 2011;155(1):10-20.PubMedGoogle ScholarCrossref
14.
Tabár  L, Faberberg  G, Day  NE, Holmberg  L.  What is the optimum interval between mammographic screening examinations? an analysis based on the latest results of the Swedish two-county breast cancer screening trial.  Br J Cancer. 1987;55(5):547-551.PubMedGoogle ScholarCrossref
15.
Tabar  L, Fagerberg  G, Chen  HH, Duffy  SW, Gad  A.  Tumour development, histology and grade of breast cancers: prognosis and progression.  Int J Cancer. 1996;66(4):413-419.PubMedGoogle ScholarCrossref
16.
Baker  LH.  Breast Cancer Detection Demonstration Project: five-year summary report.  CA Cancer J Clin. 1982;32(4):194-225.PubMedGoogle ScholarCrossref
17.
Tabár  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(8433):829-832.PubMedGoogle ScholarCrossref
18.
Buist  DS, Porter  PL, Lehman  C, Taplin  SH, White  E.  Factors contributing to mammography failure in women aged 40-49 years.  J Natl Cancer Inst. 2004;96(19):1432-1440.PubMedGoogle ScholarCrossref
19.
Anderson  TJ, Waller  M, Ellis  IO, Bobrow  L, Moss  S.  Influence of annual mammography from age 40 on breast cancer pathology.  Hum Pathol. 2004;35(10):1252-1259.PubMedGoogle ScholarCrossref
20.
White  E, Miglioretti  DL, Yankaskas  BC,  et al.  Biennial versus annual mammography and the risk of late-stage breast cancer.  J Natl Cancer Inst. 2004;96(24):1832-1839.PubMedGoogle ScholarCrossref
21.
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(8):481-492.PubMedGoogle ScholarCrossref
22.
Kerlikowske  K, Zhu  W, Hubbard  RA,  et al; Breast Cancer Surveillance Consortium.  Outcomes of screening mammography by frequency, breast density, and postmenopausal hormone therapy.  JAMA Intern Med. 2013;173(9):807-816.PubMedGoogle ScholarCrossref
23.
Dittus  K, Geller  B, Weaver  DL,  et al; Breast Cancer Surveillance Consortium.  Impact of mammography screening interval on breast cancer diagnosis by menopausal status and BMI.  J Gen Intern Med. 2013;28(11):1454-1462.PubMedGoogle ScholarCrossref
24.
Braithwaite  D, Zhu  W, Hubbard  RA,  et al; Breast Cancer Surveillance Consortium.  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(5):334-341.PubMedGoogle ScholarCrossref
25.
O’Meara  ES, Zhu  W, Hubbard  RA,  et al.  Mammographic screening interval in relation to tumor characteristics and false-positive risk by race/ethnicity and age.  Cancer. 2013;119(22):3959-3967.PubMedGoogle ScholarCrossref
26.
Coldman  A, Phillips  N, Warren  L, Kan  L.  Breast cancer mortality after screening mammography in British Columbia women.  Int J Cancer. 2007;120(5):1076-1080.PubMedGoogle ScholarCrossref
27.
Randall  D, Morrell  S, Taylor  R, Hung  WT.  Annual or biennial mammography screening for women at a higher risk with a family history of breast cancer: prognostic indicators of screen-detected cancers in New South Wales, Australia.  Cancer Causes Control. 2009;20(5):559-566.PubMedGoogle ScholarCrossref
28.
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(3):339-345.PubMedGoogle ScholarCrossref
29.
van Ravesteyn  NT, Miglioretti  DL, Stout  NK,  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(9):609-617.PubMedGoogle ScholarCrossref
30.
Stout  NK, Lee  SJ, Schechter  CB,  et al.  Benefits, harms, and costs for breast cancer screening after US implementation of digital mammography.  J Natl Cancer Inst. 2014;106(6):dju092.PubMedGoogle ScholarCrossref
31.
O’Donoghue  C, Eklund  M, Ozanne  EM, Esserman  LJ.  Aggregate cost of mammography screening in the United States: comparison of current practice and advocated guidelines.  Ann Intern Med. 2014;160(3):145-153.PubMedGoogle Scholar
32.
Ballard-Barbash  R, Taplin  SH, Yankaskas  BC,  et al; Breast Cancer Surveillance Consortium.  Breast Cancer Surveillance Consortium: a national mammography screening and outcomes database.  AJR Am J Roentgenol. 1997;169(4):1001-1008.PubMedGoogle ScholarCrossref
33.
Sickles  EA, Miglioretti  DL, Ballard-Barbash  R,  et al.  Performance benchmarks for diagnostic mammography.  Radiology. 2005;235(3):775-790.PubMedGoogle ScholarCrossref
34.
Ernster  VL, Ballard-Barbash  R, Barlow  WE,  et al.  Detection of ductal carcinoma in situ in women undergoing screening mammography.  J Natl Cancer Inst. 2002;94(20):1546-1554.PubMedGoogle ScholarCrossref
35.
Breast Cancer Surveillance Consortium.  BCSC Glossary of Terms. 2009.http://breastscreening.cancer.gov/data/bcsc_data_definitions.pdf. Accessed March 9, 2015.
36.
Phipps  AI, Ichikawa  L, Bowles  EJ,  et al.  Defining menopausal status in epidemiologic studies: a comparison of multiple approaches and their effects on breast cancer rates.  Maturitas. 2010;67(1):60-66.PubMedGoogle ScholarCrossref
37.
Kerlikowske  K, Miglioretti  DL, Ballard-Barbash  R,  et al.  Prognostic characteristics of breast cancer among postmenopausal hormone users in a screened population.  J Clin Oncol. 2003;21(23):4314-4321.PubMedGoogle ScholarCrossref
38.
Greene  FL, Page  DL, Fleming  ID,  et al.  AJCC Cancer Staging Manual. 6th ed. New York, NY: Springer-Verlag; 2002.
39.
McNutt  LA, Wu  C, Xue  X, Hafner  JP.  Estimating the relative risk in cohort studies and clinical trials of common outcomes.  Am J Epidemiol. 2003;157(10):940-943.PubMedGoogle ScholarCrossref
40.
Carney  PA, Miglioretti  DL, Yankaskas  BC,  et al.  Individual and combined effects of age, breast density, and hormone replacement therapy use on the accuracy of screening mammography.  Ann Intern Med. 2003;138(3):168-175.PubMedGoogle ScholarCrossref
41.
Kerlikowske  K, Ichikawa  L, Miglioretti  DL,  et al; National Institutes of Health Breast Cancer Surveillance Consortium.  Longitudinal measurement of clinical mammographic breast density to improve estimation of breast cancer risk.  J Natl Cancer Inst. 2007;99(5):386-395.PubMedGoogle ScholarCrossref
42.
Pisano  ED, Gatsonis  C, Hendrick  E,  et al; Digital Mammographic Imaging Screening Trial (DMIST) Investigators Group.  Diagnostic performance of digital versus film mammography for breast-cancer screening.  N Engl J Med. 2005;353(17):1773-1783.PubMedGoogle ScholarCrossref
43.
Pisano  ED, Hendrick  RE, Yaffe  MJ,  et al; DMIST Investigators Group.  Diagnostic accuracy of digital versus film mammography: exploratory analysis of selected population subgroups in DMIST.  Radiology. 2008;246(2):376-383.PubMedGoogle ScholarCrossref
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    1 Comment for this article
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    Observations on Observational study limitations
    Robert Rosenberg MD FACR, David Seidenwurm MD FACR | Professor Emeritus University of New Mexico, Diagnostic Imaging Sutter Health Sacramento CA
    Miglioretti et al (ref 1) report an observational study of annual mammography versus biennial mammography. The paper does not recognize that there are many reasons for variation in intervals of screening related to behavioral, demographic and medical factors that may influence the comparison. One such omission is the use of breast imaging between screening studies, another is the timeliness of women to return for health care due to symptoms. Women with more frequent studies in the follow up period would have lower stage cancers than those with fewer studies. These represent uncorrected confounders.



    The similar sensitivity of mammography in the
    two groups - ~76% and 72%, is an indication of an observational study problem. Typically, there is a greater sensitivity difference between annual and biennial screening because many more interval cancers occur in the second year compared to the first year. An earlier report from the Breast Cancer Surveillance Consortium using slightly different methods showed greater differences between annual and biennial screening – 74% vs 62% (Ref 2) as does a report from the UK (Fig 1 of Ref 3).



    Several possible explanations exist for the discrepancy:

    1) missing interval cancers in the biennial screening group due to delayed care or more patients lost to follow up,

    2) less than 2 year follow up in the biennial group due to early screening in the second year (by definition - early screens truncate follow up and cancers are not interval cancers), and 3) other differences in the health care use or access of the two groups.



    Available metrics to assess these potential confounders that are included in the Consortium data include comparison of use of diagnostic and breast imaging between screening examinations, and comparison of the total cancers including interval and screen detected cancers in the two populations over a two-year period of time.



    Therefore, this paper likely systematically underestimates the differences of annual vs. biennial screening.

    1) Miglioretti DL, Zhu W, Kerlikowske K, et.al. Breast Tumor Prognostic Characteristics and Biennial vs Annual Mammography, Age, and Menopausal Status. JAMA Oncol. 2015;1(8):1069-1077. doi:10.1001/jamaoncol.2015.3084.

    2) Bennett RL, Sellars SJ, Moss SM. Interval cancers in the NHS breast cancer screening programme in England, Wales and Northern Ireland. British Journal of Cancer (2011) 104, 571 – 577.

    3) White, E, Miglioretti, DL, Yankaskas, BC, et al. Biennial versus annual mammography and the risk of late-stage breast cancer. JNCI; DEC 15 2004; v.96, no.24, p.1832-183.
    CONFLICT OF INTEREST: None Reported
    READ MORE
    Original Investigation
    November 2015

    Breast Tumor Prognostic Characteristics and Biennial vs Annual Mammography, Age, and Menopausal Status

    Author Affiliations
    • 1Division of Biostatistics, Department of Public Health Sciences, University of California Davis School of Medicine, Davis
    • 2Group Health Research Institute, Group Health Cooperative, Seattle, Washington
    • 3Departments of Medicine and Epidemiology and Biostatistics, University of California–San Francisco, San Francisco,
    • 4General Internal Medicine Section, Department of Veterans Affairs, University of California–San Francisco, San Francisco
    • 5Department of Surgery, Office of Health Promotion Research, University of Vermont College of Medicine, Burlington
    • 6University of Vermont Cancer Center, University of Vermont College of Medicine, Burlington
    • 7Department of Biomedical Data Science, Geisel School of Medicine at Dartmouth, Lebanon, New Hampshire
    • 8Department of Epidemiology, Geisel School of Medicine at Dartmouth, Lebanon, New Hampshire
    • 9Department of Radiology, The University of North Carolina, Chapel Hill
    • 10Cancer Control Science Department, American Cancer Society, Atlanta, Georgia
    JAMA Oncol. 2015;1(8):1069-1077. doi:10.1001/jamaoncol.2015.3084
    Abstract

    Importance  Screening mammography intervals remain under debate in the United States.

    Objective  To compare the proportion of breast cancers with less vs more favorable prognostic characteristics in women screening annually vs biennially by age, menopausal status, and postmenopausal hormone therapy (HT) use.

    Design, Setting, and Participants  This was a study of a prospective cohort from 1996 to 2012 at Breast Cancer Surveillance Consortium facilities. A total of 15 440 women ages 40 to 85 years with breast cancer diagnosed within 1 year of an annual or within 2 years of a biennial screening mammogram.

    Exposures  We updated previous analyses by using narrower intervals for defining annual (11-14 months) and biennial (23-26 months) screening.

    Main Outcomes and Measures  We defined less favorable prognostic characteristics as tumors that were stage IIB or higher, size greater than 15 mm, positive nodes, and any 1 or more of these characteristics. We used log-binomial regression to model the proportion of breast cancers with less favorable characteristics following a biennial vs annual screen by 10-year age groups and by menopausal status and current postmenopausal HT use.

    Results  Among 15 440 women with breast cancer, most were 50 years or older (13 182 [85.4%]), white (12 063 [78.1%]), and postmenopausal (9823 [63.6%]). Among 2027 premenopausal women (13.1%), biennial screeners had higher proportions of tumors that were stage IIB or higher (relative risk [RR], 1.28 [95% CI, 1.01-1.63]; P = .04), size greater than 15 mm (RR, 1.21 [95% CI, 1.07-1.37]; P = .002), and with any less favorable prognostic characteristic (RR, 1.11 [95% CI, 1.00-1.22]; P = .047) compared with annual screeners. Among women currently taking postmenopausal HT, biennial screeners tended to have tumors with less favorable prognostic characteristics compared with annual screeners; however, 95% CIs were wide, and differences were not statistically significant (for stage 2B+, RR, 1.14 [95% CI, 0.89-1.47], P = .29; size >15 mm, RR, 1.13 [95% CI, 0.98-1.31], P = .09; node positive, RR, 1.18 [95% CI, 0.98-1.42], P = .09; any less favorable characteristic, RR, 1.12 [95% CI, 1.00-1.25], P = .053). The proportions of tumors with less favorable prognostic characteristics were not significantly larger for biennial vs annual screeners among postmenopausal women not taking HT (eg, any characteristic: RR, 1.03 [95% CI, 0.95-1.12]; P = .45), postmenopausal HT users after subdividing by type of hormone use (eg, any characteristic: estrogen + progestogen users, RR, 1.16 [95% CI, 0.91-1.47]; P = .22; estrogen-only users, RR, 1.14 [95% CI, 0.94-1.37]; P = .18), or any 10-year age group (eg, any characteristic: ages 40-49 years, RR, .1.04 [95% CI, 0.94-1.14]; P = .48; ages 50-59 years, RR, 1.03 [95% CI, 0.94-1.12]; P = .58; ages 60-69 years, RR, 1.07 [95% CI, 0.97-1.19]; P = .18; ages 70-85 years, RR, 1.05 [95% CI, 0.94-1.18]; P = .35).

    Conclusions and Relevance  Premenopausal women diagnosed as having breast cancer following biennial vs annual screening mammography are more likely to have tumors with less favorable prognostic characteristics. Postmenopausal women not using HT who are diagnosed as having breast cancer following a biennial or annual screen have similar proportions of tumors with less favorable prognostic characteristics.

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