Breast Cancer Research and Treatment

, Volume 143, Issue 3, pp 541–550 | Cite as

Factors associated with long-term adherence to annual surveillance mammography among breast cancer survivors

  • Heidi S. Wirtz
  • Denise M. Boudreau
  • Julie R. Gralow
  • William E. Barlow
  • Shelly Gray
  • Erin J. A. Bowles
  • Diana S. M. Buist


Clinical practice guidelines recommend yearly surveillance mammography for breast cancer survivors, yet many women do not receive this service. The objective of this study was to evaluate factors related to long-term surveillance mammography adherence among breast cancer survivors. We conducted a retrospective cohort study among women ≥18 years, diagnosed with incident stage I or II breast cancer between 1990 and 2008. We used medical record and administrative health plan data to ascertain covariates and receipt of surveillance mammography for up to 10 years after completing breast cancer treatment. Surveillance included post-diagnosis screening exams among asymptomatic women. We used multivariable repeated measures generalized estimating equation regression models to estimate odds ratios and robust 95 % confidence intervals to examine factors related to the annual receipt of surveillance mammography. The analysis included 3,965 women followed for a median of six surveillance years; 79 % received surveillance mammograms in year 1 but decreased to 63 % in year 10. In multivariable analyses, women, who were <40 years or 80+ years of age (compared to 50–59 years), current smokers, had greater comorbidity, were diagnosed more recently, had stage II cancer, or were treated with mastectomy or breast conserving surgery without radiation, were less likely than other women to receive surveillance mammography. Women with outpatient visits during the year to primary care providers, oncologists, or both were more likely to undergo surveillance. In this large cohort study of women diagnosed with early-stage invasive breast cancer, we found that important subgroups of women are at high risk for non-adherence to surveillance recommendations, even among younger breast cancer survivors. Efforts should be undertaken to actively engage breast cancer survivors in managing long-term surveillance care.


Breast cancer Cancer survivors Surveillance Mammography Survivorship care 

Supplementary material

10549_2013_2816_MOESM1_ESM.doc (310 kb)
Supplementary material 1 (DOC 310 kb)


  1. 1.
    Howlader N, Noone AM, Krapcho M, et al (2011) SEER Cancer Statistics Review, 1975–2008, National Cancer Institute. Accessed 11 June 2011
  2. 2.
    Lash TL, Fox MP, Buist DS et al (2007) Mammography surveillance and mortality in older breast cancer survivors. J Clin Oncol 25:3001–3006. doi:10.1200/JCO.2006.09.9572 PubMedCrossRefGoogle Scholar
  3. 3.
    Carlson RW, Allred DC, Anderson BO et al (2011) Invasive breast cancer. J Natl Compr Canc Netw 9:136–222PubMedGoogle Scholar
  4. 4.
    Khatcheressian JL, Hurley P, Bantug E et al (2013) Breast cancer follow-up and management after primary treatment: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol 31:961–965. doi:10.1200/JCO.2012.45.9859 PubMedCrossRefGoogle Scholar
  5. 5.
    Field TS, Doubeni C, Fox MP et al (2008) Under utilization of surveillance mammography among older breast cancer survivors. J Gen Intern Med 23:158–163. doi:10.1007/s11606-007-0471-2 PubMedCentralPubMedCrossRefGoogle Scholar
  6. 6.
    Andersen MR, Urban N (1998) The use of mammography by survivors of breast cancer. Am J Public Health 88:1713–1715PubMedCrossRefGoogle Scholar
  7. 7.
    Geller BM, Kerlikowske K, Carney PA et al (2003) Mammography surveillance following breast cancer. Breast Cancer Res Treat 81:107–115. doi:10.1023/A:1025794629878 PubMedCrossRefGoogle Scholar
  8. 8.
    Lash TL, Silliman RA (2001) Medical surveillance after breast cancer diagnosis. Med Care 39:945–955PubMedCrossRefGoogle Scholar
  9. 9.
    Schapira MM, McAuliffe TL, Nattinger AB (2000) Underutilization of mammography in older breast cancer survivors. Med Care 38:281–289PubMedCrossRefGoogle Scholar
  10. 10.
    Keating NL, Landrum MB, Guadagnoli E et al (2006) Factors related to underuse of surveillance mammography among breast cancer survivors. J Clin Oncol 24:85–94. doi:10.1200/JCO.2005.02.4174 PubMedCrossRefGoogle Scholar
  11. 11.
    Doubeni CA, Field TS, Ulcickas Yood M et al (2006) Patterns and predictors of mammography utilization among breast cancer survivors. Cancer 106:2482–2488. doi:10.1002/cncr.21893 PubMedCrossRefGoogle Scholar
  12. 12.
    Demicheli R, Biganzoli E, Boracchi P et al (2008) Recurrence dynamics does not depend on the recurrence site. Breast Cancer Res 10:R83. doi:10.1186/bcr2152 PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Retsky M, Demicheli R, Hrushesky WJ (2005) Does surgery induce angiogenesis in breast cancer? Indirect evidence from relapse pattern and mammography paradox. Int J Surg 3:179–187. doi:10.1016/j.ijsu.2005.08.002 PubMedCrossRefGoogle Scholar
  14. 14.
    Wirtz HS, Buist DS, Gralow JR et al (2013) Frequent antibiotic use and second breast cancer events. Cancer Epidemiol Biomarkers Prev 22(9):1588–1599. doi:10.1158/1055-9965.EPI-13-0454 PubMedCrossRefGoogle Scholar
  15. 15.
    Greene FL, Page DL, Fleming ID et al (2002) AJCC cancer staging manual, 6th edn. Springer, New YorkCrossRefGoogle Scholar
  16. 16.
    Chubak J, Buist DS, Boudreau DM et al (2008) Breast cancer recurrence risk in relation to antidepressant use after diagnosis. Breast Cancer Res Treat 112:123–132. doi:10.1007/s10549-007-9828-9 PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    Geiger AM, Thwin SS, Lash TL et al (2007) Recurrences and second primary breast cancers in older women with initial early-stage disease. Cancer 109:966–974. doi:10.1002/cncr.22472 PubMedCrossRefGoogle Scholar
  18. 18.
    Calip GS, Boudreau DM, Loggers ET (2013) Changes in adherence to statins and subsequent lipid profiles during and following breast cancer treatment. Breast Cancer Res Treat 138:225–233. doi:10.1007/s10549-013-2424-2 PubMedCrossRefGoogle Scholar
  19. 19.
    Taplin SH, Thompson RS, Schnitzer F et al (1990) Revisions in the risk-based Breast Cancer Screening Program at Group Health Cooperative. Cancer 66:812–818PubMedCrossRefGoogle Scholar
  20. 20.
    Group Health Research Institute (2012) Group Health Breast Cancer Surveillance Registry. Accessed 9 July 2013
  21. 21.
    Saunders KW, Davis RL, Stergachis A (2005) Group Health Cooperative. In: Strom BL (ed) Pharmacoepidemiology, 4th edn. Wiley, West Sussex, pp 223–239Google Scholar
  22. 22.
    Houssami N, Abraham LA, Miglioretti DL et al (2011) Accuracy and outcomes of screening mammography in women with a personal history of early-stage breast cancer. JAMA 305:790–799. doi:10.1001/jama.2011.188 PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Phipps AI, Ichikawa L, Bowles EJ et al (2010) Defining menopausal status in epidemiologic studies: a comparison of multiple approaches and their effects on breast cancer rates. Maturitas 67:60–66. doi:10.1016/j.maturitas.2010.04.015 PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Deyo RA, Cherkin DC, Ciol MA (1992) Adapting a clinical comorbidity index for use with ICD-9-CM administrative databases. J Clin Epidemiol 45:613–619PubMedCrossRefGoogle Scholar
  25. 25.
    Zeger SL, Liang KY (1986) Longitudinal data analysis for discrete and continuous outcomes. Biometrics 42:121–130PubMedCrossRefGoogle Scholar
  26. 26.
    Hudis CA, Barlow WE, Costantino JP et al (2007) Proposal for standardized definitions for efficacy end points in adjuvant breast cancer trials: the STEEP system. J Clin Oncol 25:2127–2132. doi:10.1200/JCO.2006.10.3523 PubMedCrossRefGoogle Scholar
  27. 27.
    Onega T, Weiss J, Diflorio R et al (2012) Evaluating surveillance breast imaging and biopsy in older breast cancer survivors. Int J Breast Cancer 2012:347646. doi:10.1155/2012/347646 PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Buist DS, Abraham LA, Barlow WE et al (2010) Diagnosis of second breast cancer events after initial diagnosis of early stage breast cancer. Breast Cancer Res Treat 124:863–873. doi:10.1007/s10549-010-1106-6 PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Jackson LA, Nelson JC, Benson P et al (2006) Functional status is a confounder of the association of influenza vaccine and risk of all cause mortality in seniors. Int J Epidemiol 35:345–352. doi:10.1093/ije/dyi275 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Heidi S. Wirtz
    • 1
  • Denise M. Boudreau
    • 1
    • 2
  • Julie R. Gralow
    • 3
  • William E. Barlow
    • 4
    • 5
  • Shelly Gray
    • 1
  • Erin J. A. Bowles
    • 2
  • Diana S. M. Buist
    • 2
    • 6
    • 7
  1. 1.Department of PharmacyUniversity of WashingtonSeattleUSA
  2. 2.Group Health Research InstituteSeattleUSA
  3. 3.Seattle Cancer Care AllianceSeattleUSA
  4. 4.Cancer Research and BiostatisticsSeattleUSA
  5. 5.Department of BiostatisticsUniversity of WashingtonSeattleUSA
  6. 6.Department of EpidemiologyUniversity of WashingtonSeattleUSA
  7. 7.Department of Health ServicesUniversity of WashingtonSeattleUSA

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