Journal of General Internal Medicine

, Volume 28, Issue 11, pp 1454–1462 | Cite as

Impact of Mammography Screening Interval on Breast Cancer Diagnosis by Menopausal Status and BMI

  • Kim Dittus
  • Berta Geller
  • Donald L. Weaver
  • Karla Kerlikowske
  • Weiwei Zhu
  • Rebecca Hubbard
  • Dejana Braithwaite
  • Ellen S. O’Meara
  • Diana L. Miglioretti
  • For the Breast Cancer Surveillance Consortium



Controversy remains regarding the frequency of screening mammography. Women with different risks for developing breast cancer because of body mass index (BMI) may benefit from tailored recommendations.


To determine the impact of mammography screening interval for women who are normal weight (BMI < 25), overweight (BMI 25–29.9), or obese (BMI ≥ 30), stratified by menopausal status.


Two cohorts selected from the Breast Cancer Surveillance Consortium. Patient and mammography data were linked to pathology databases and tumor registries.


The cohort included 4,432 women aged 40–74 with breast cancer; the false-positive analysis included a cohort of 553,343 women aged 40–74 without breast cancer.


Stage, tumor size and lymph node status by BMI and screening interval (biennial vs. annual). Cumulative probability of false-positive recall or biopsy by BMI and screening interval. Analyses were stratified by menopausal status.


Premenopausal obese women undergoing biennial screening had a non-significantly increased odds of a tumor size > 20 mm relative to annual screeners (odds ratio [OR] = 2.07; 95 % confidence interval [CI] 0.997 to 4.30). Across all BMI categories from normal to obese, postmenopausal women with breast cancer did not present with higher stage, larger tumor size or node positive tumors if they received biennial rather than annual screening. False-positive recall and biopsy recommendations were more common among annually screened women.


The only negative outcome identified for biennial vs. annual screening was a larger tumor size (> 20 mm) among obese premenopausal women. Since annual mammography does not improve stage at diagnosis compared to biennial screening and false-positive recall/biopsy rates are higher with annual screening, women and their primary care providers should weigh the harms and benefits when deciding on annual versus biennial screening.


mammography BMI menopausal status 


  1. 1.
    Nelson HD, Tyne K, Naik A, et al. Screening for breast cancer: an update for the U.S. Preventive Services Task Force. Ann Intern Med. 2009;151:727–37, W237–42.Google Scholar
  2. 2.
    Gotzsche PC, Nielsen M. Screening for breast cancer with mammography. Cochrane Database Syst Rev. 2011;1, CD001877.PubMedGoogle Scholar
  3. 3.
    Fletcher SW, Elmore JG. Clinical practice. Mammographic screening for breast cancer. N Engl J Med. 2003;348:1672–80.PubMedCrossRefGoogle Scholar
  4. 4.
    Blamey RW. The frequency of breast cancer screening: results from the UKCCCR randomized trial. Eur J Cancer. 2002;38:1458–64.CrossRefGoogle Scholar
  5. 5.
    Calonge N, Petitti D, DeWitt T, et al. Screening for breast cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2009;151:716–26, W-236.Google Scholar
  6. 6.
    Smith RA, Cokkinides V, Brooks D, et al. Cancer screening in the United States, 2010: a review of current American Cancer Society guidelines and issues in cancer screening. CA Cancer J Clin. 2010;60:99–119.PubMedCrossRefGoogle Scholar
  7. 7.
    ACOG. Annual Mammograms Now Recommended for Women Beginning at Age 402011: Available from:
  8. 8.
    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.PubMedCrossRefGoogle Scholar
  9. 9.
    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.PubMedCrossRefGoogle Scholar
  10. 10.
    Hunt KA, Sickles EA. Effect of obesity on screening mammography: outcomes analysis of 88,346 consecutive examinations. AJR Am J Roentgenol. 2000;174:1251–5.PubMedCrossRefGoogle Scholar
  11. 11.
    Cui Y, Whiteman MK, Flaws JA, et al. Body mass and stage of breast cancer at diagnosis. Int J Cancer. 2002;98:279–83.PubMedCrossRefGoogle Scholar
  12. 12.
    Porter GA, Inglis KM, Wood LA, et al. Effect of obesity on presentation of breast cancer. Ann Surg Oncol. 2006;13:327–32.PubMedCrossRefGoogle Scholar
  13. 13.
    Ahn J, Schatzkin A, Lacey JV Jr, et al. Adiposity, adult weight change, and postmenopausal breast cancer risk. Arch Intern Med. 2007;167:2091–102.PubMedCrossRefGoogle Scholar
  14. 14.
    Daling JR, Malone KE, Doody DR, et al. Relation of body mass index to tumor markers and survival among young women with invasive ductal breast carcinoma. Cancer. 2001;92:720–9.PubMedCrossRefGoogle Scholar
  15. 15.
    Macinnis RJ, English DR, Gertig DM, et al. Body size and composition and risk of postmenopausal breast cancer. Cancer Epidemiol Biomarkers Prev. 2004;13:2117–25.PubMedGoogle Scholar
  16. 16.
    Feigelson HS, Patel AV, Teras LR, et al. Adult weight gain and histopathologic characteristics of breast cancer among postmenopausal women. Cancer. 2006;107:12–21.PubMedCrossRefGoogle Scholar
  17. 17.
    Stark A, Stahl MS, Kirchner HL, et al. Body mass index at the time of diagnosis and the risk of advanced stages and poorly differentiated cancers of the breast: findings from a case-series study. Int J Obes (Lond). 2010;34:1381–6.CrossRefGoogle Scholar
  18. 18.
    Kerlikowske K, Walker R, Miglioretti DL, et al. Obesity, mammography use and accuracy, and advanced breast cancer risk. J Natl Cancer Inst. 2008;100:1724–33.PubMedCrossRefGoogle Scholar
  19. 19.
    Renehan AG, Frystyk J, Flyvbjerg A. Obesity and cancer risk: the role of the insulin-IGF axis. Trends Endocrinol Metab. 2006;17:328–36.PubMedCrossRefGoogle Scholar
  20. 20.
    Gonullu G, Ersoy C, Ersoy A, et al. Relation between insulin resistance and serum concentrations of IL-6 and TNF-alpha in overweight or obese women with early stage breast cancer. Cytokine. 2005;31:264–9.PubMedCrossRefGoogle Scholar
  21. 21.
    Garofalo C, Koda M, Cascio S, et al. Increased expression of leptin and the leptin receptor as a marker of breast cancer progression: possible role of obesity-related stimuli. Clin Cancer Res. 2006;12:1447–53.PubMedCrossRefGoogle Scholar
  22. 22.
    Ostbye T, Taylor DH Jr, Yancy WS Jr, et al. Associations between obesity and receipt of screening mammography, Papanicolaou tests, and influenza vaccination: results from the Health and Retirement Study (HRS) and the Asset and Health Dynamics Among the Oldest Old (AHEAD) Study. Am J Public Health. 2005;95:1623–30.PubMedCrossRefGoogle Scholar
  23. 23.
    Maruthur NM, Bolen S, Brancati FL, et al. Obesity and mammography: a systematic review and meta-analysis. J Gen Intern Med. 2009;24:665–77.PubMedCrossRefGoogle Scholar
  24. 24.
    Nelson HD, Zakher B, Cantor A, Fu R, Grivvin J, O’Meara ES, Buist DSM, Kerlikowske K, van Ravesteyn NT, Trentham-Dietz A, Mandelblatt JS, Miglioretti DS. Risk factors for breast cancer for women aged 40–49 years: a systemic review and metaanalysis. Ann Intern Med. 2012;156:635–48.PubMedCrossRefGoogle Scholar
  25. 25.
    Elmore JG, Carney PA, Abraham LA, et al. The association between obesity and screening mammography accuracy. Arch Intern Med. 2004;164:1140–7.PubMedCrossRefGoogle Scholar
  26. 26.
    Destounis S, Newell M, Pinsky R. Breast imaging and intervention in the overweight and obese patient. AJR Am J Roentgenol. 2011;196:296–302.PubMedCrossRefGoogle Scholar
  27. 27.
    Ballard-Barbash R, Taplin SH, Yankaskas BC, et al. Breast Cancer Surveillance Consortium: a national mammography screening and outcomes database. Am J Roentgenol. 1997;169:1001–8.CrossRefGoogle Scholar
  28. 28.
    American College of Radiology. Breast Imaging Reporting and Data System (BI-RADS) Breast Imaging Atlas. Reston: American College of Radiology; 2003.Google Scholar
  29. 29.
    Ernster VL, Ballard-Barbash R, Barlow WE, Zheng Y, Weaver DL, Cutter G, Yankaskas BC, Rosenberg R, Carney PA, Kerlikowske K, Taplin SH, Urban N, Geller BM. Detection of ductal carcinoma in situ in women undergoing screening mammography. J Natl Cancer Inst. 2002;94(20):1546–54.PubMedCrossRefGoogle Scholar
  30. 30.
    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;96:1832–9.PubMedCrossRefGoogle Scholar
  31. 31.
    Sprague BL, Trentham-Dietz A, Cronin KA. A sustained decline in postmenopausal hormone use: results from the National Health and Nutrition Examination Survey, 1999–2010. Obstet Gynecol. 2012;120(3):595–603.PubMedCrossRefGoogle Scholar
  32. 32.
    NHLBI. Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults—the evidence report. National Institutes of Health. Obes Res. 1998;6:51S–209.CrossRefGoogle Scholar
  33. 33.
    American Joint Committee on Cancer. Manual for Staging of Cancer. 6th ed. Philadelphia: JB Lippincott; 2002.Google Scholar
  34. 34.
    Rothman KJ. No adjustments are needed for multiple comparisons. Epidemiology. 1990;1(1):43–6.PubMedCrossRefGoogle Scholar
  35. 35.
    Hubbard RA, Miglioretti DL, Smith RA. Modelling the cumulative risk of a false-positive screening test. Stat Methods Med Res. 2010;19:429–49.PubMedCrossRefGoogle Scholar
  36. 36.
    Allred DC. Ductal carcinoma in situ: terminology, classification, and natural history. J Natl Cancer Inst Monogr. 2010;2010:134–8.PubMedCrossRefGoogle Scholar
  37. 37.
    Page DL, Dupont WD, Rogers LW, et al. Continued local recurrence of carcinoma 15–25 years after a diagnosis of low grade ductal carcinoma in situ of the breast treated only by biopsy. Cancer. 1995;76:1197–2000.PubMedCrossRefGoogle Scholar
  38. 38.
    Kerlikowske K, Molinaro A, Cha I, et al. Characteristics associated with recurrence among women with ductal carcinoma in situ treated by lumpectomy. J Natl Cancer Inst. 2003;95:1692–702.PubMedCrossRefGoogle Scholar
  39. 39.
    Kerlikowske K, Molinaro AM, Gauthier ML, et al. Biomarker expression and risk of subsequent tumors after initial ductal carcinoma in situ diagnosis. J Natl Cancer Inst. 2010;102:627–37.PubMedCrossRefGoogle Scholar
  40. 40.
    Yaffe MJ, Mainprize JG. Risk of radiation-induced breast cancer from mammographic screening. Radiology. 2011;258:98–105.PubMedCrossRefGoogle Scholar
  41. 41.
    Flegal KM, Carroll MD, Ogden CL, et al. Prevalence and trends in obesity among US adults, 1999–2008. JAMA. 2010;303:235–41.PubMedCrossRefGoogle Scholar
  42. 42.
    Merrill RM, Richardson JS. Validity of self-reported height, weight, and body mass index: findings from the National Health and Nutrition Examination Survey, 2001–2006. Prev Chronic Dis. 2009;6:A121.PubMedGoogle Scholar
  43. 43.
    Sickles EA, Miglioretti DL, Ballard-Barbash R, Geller BM, Leung JWT, Rosenberg RD, Smith-Blindman R, Yankaskas BC. Performance benchmarks for diagnostic mammography. Radiology. 2005;253(3):775–90.CrossRefGoogle Scholar
  44. 44.
    Henry LR, Stojadinovic A, Swain SM, et al. The influence of a gene expression profile on breast cancer decisions. J Surg Oncol. 2009;99:319–23.PubMedCrossRefGoogle Scholar
  45. 45.
    Lo SS, Mumby PB, Norton J, et al. Prospective multicenter study of the impact of the 21-gene recurrence score assay on medical oncologist and patient adjuvant breast cancer treatment selection. J Clin Oncol. 2010;28:1671–6.PubMedCrossRefGoogle Scholar
  46. 46.
    Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63:11–20.PubMedCrossRefGoogle Scholar

Copyright information

© Society of General Internal Medicine 2013

Authors and Affiliations

  • Kim Dittus
    • 1
  • Berta Geller
    • 2
  • Donald L. Weaver
    • 3
  • Karla Kerlikowske
    • 4
  • Weiwei Zhu
    • 5
  • Rebecca Hubbard
    • 5
    • 6
  • Dejana Braithwaite
    • 4
  • Ellen S. O’Meara
    • 5
  • Diana L. Miglioretti
    • 5
    • 7
  • For the Breast Cancer Surveillance Consortium
  1. 1.Departments of Hematology/OncologyUniversity of Vermont, College of MedicineBurlingtonUSA
  2. 2.Family Medicine and Radiology DepartmentsUniversity of Vermont, College of MedicineBurlingtonUSA
  3. 3.Department of PathologyUniversity of Vermont, College of MedicineBurlingtonUSA
  4. 4.Departments of Medicine and Epidemiology and BiostatisticsUniversity of CaliforniaSan FranciscoUSA
  5. 5.Group Health Research Institute, Group Health CooperativeSeattleUSA
  6. 6.Department of BiostatisticsUniversity of WashingtonSeattleUSA
  7. 7.Division of Biostatistics, Department of Public Health SciencesUniversity of California Davis School of MedicineDavisUSA

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