Advertisement

Breast Cancer Research and Treatment

, Volume 142, Issue 1, pp 153–163 | Cite as

Long-term surveillance mammography and mortality in older women with a history of early stage invasive breast cancer

  • Diana S. M. BuistEmail author
  • Jaclyn L. F. Bosco
  • Rebecca A. Silliman
  • Heather Taffet Gold
  • Terry Field
  • Marianne Ulcickas Yood
  • Virginia P. Quinn
  • Marianne Prout
  • Timothy L. Lash
  • The Breast Cancer Outcomes in Older Women (BOW) Investigators
Epidemiology

Abstract

Annual surveillance mammograms in older long-term breast cancer survivors are recommended, but this recommendation is based on little evidence and with no guidelines on when to stop. Surveillance mammograms should decrease breast cancer mortality by detecting second breast cancer events at an earlier stage. We examined the association between surveillance mammography beyond 5 years after diagnosis on breast cancer-specific mortality in a cohort of women aged ≥65 years diagnosed 1990–1994 with early stage breast cancer. Our cohort included women who survived disease free for ≥5 years (N = 1,235) and were followed from year 6 through death, disenrollment, or 15 years after diagnosis. Asymptomatic surveillance mammograms were ascertained through medical record review. We used Cox proportional hazards regression stratified by follow-up year to calculate the association between time-varying surveillance mammography and breast cancer-specific and other-than-breast mortality adjusting for site, stage, primary surgery type, age and time-varying Charlson Comorbidity Index. The majority (85 %) of the 1,235 5-year breast cancer survivors received ≥1 surveillance mammogram in years 5–9 (yearly proportions ranged from 48 to 58 %); 82 % of women received ≥1 surveillance mammogram in years 10–14. A total of 120 women died of breast cancer and 393 women died from other causes (average follow-up 7.3 years). Multivariable models and lasagna plots suggested a modest reduction in breast cancer-specific mortality with surveillance mammogram receipt in the preceding year (IRR 0.82, 95 % CI 0.56–1.19, p = 0.29); the association with other-cause mortality was 0.95 (95 % CI 0.78–1.17, p = 0.64). Among older breast cancer survivors, surveillance mammography may reduce breast cancer-specific mortality even after 5 years of disease-free survival. Continuing surveillance mammography in older breast cancer survivors likely requires physician–patient discussions similar to those recommended for screening, taking into account comorbid conditions and life-expectancy.

Keywords

Surveillance mammography Breast carcinoma Survivorship 

Notes

Acknowledgments

Supported by a grant from the National Cancer Institute (R01 CA093772 R. Silliman, PI). The CRN is a consortium of 14 integrated health care delivery systems with more than 10 million enrollees. The overall goal of the CRN is to assess and increase the effectiveness of preventive, curative and supportive interventions for major cancers through a program of collaborative research among diverse populations and health systems. We would like to thank site principal investigators Hans Petersen and Meaghan St. Charles from Lovelace Clinic Foundation and Pamala Pawloski from Heath Partners and Hongyuan Gao for her work developing the lasagna plots. We would also like to thank our site project managers, programmers, and medical record abstractors: Group Health-Linda Shultz, Kristin Delaney, Margaret Farrell-Ross, Mary Sunderland, Millie Magner, and Beth Kirlin; Meyers Primary Care Institute and Fallon Clinic-Jackie Fuller, Doris Hoyer, and Janet Guilbert; Henry Ford Health System-Sharon Hensley Alford, Karen Wells, Patricia Baker, and Rita Montague; HealthPartners-Maribet McCarty and Alex Kravchik; Kaiser Permanente Southern California-Julie Stern, Janis Yao, Michelle McGuire, and Erica Hnatek-Mitchell; and Lovelace Health Plan-Judith Hurley, Hans Petersen, and Melissa Roberts.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Surveillance epidemiology and end results relative survival by survival time by age at diagnosis/death female breast, all races, female 1988–2008 National Cancer Institute. http://seer.cancer.gov/faststats/selections.php?run=runit&output=2&data=4&statistic=5&cancer=553&year=201204&race=1&sex=3&series=age&age=166#Output. Accessed 20 Aug 2013
  2. 2.
    Reis LAG, Eisner MP (2007) Cancer of the female breast. In: Reis LAG, Young JL, Keel GE, Eisner MP, Lin YD, Horner MJ (eds) SEER survival monograph: cancer survival among adults: US SEER program, 1988–2001, Patient and tumor characteristics. National Cancer Institute, SEER Program, Bethesda, pp 101–111 NIH Pub. No. 07-6215Google Scholar
  3. 3.
    Arias E (2011) United States life tables, 2007. Natl Vital Stat Rep 59:1–61PubMedGoogle Scholar
  4. 4.
    Walter LC, Covinsky KE (2001) Cancer screening in elderly patients: a framework for individualized decision making. JAMA 285:2750–2756PubMedCrossRefGoogle Scholar
  5. 5.
    Weiss NS (2011) The analysis of case-control studies of the efficacy of screening for recurrence of cancer. J Clin Epidemiol 64:41–43. doi: 10.1016/j.jclinepi.2010.07.013 PubMedCrossRefGoogle Scholar
  6. 6.
    National Comprehensive Cancer Network (2012) National Comprehensive Cancer Network: NCCN Guidelines. National Comprehensive Cancer Network. http://www.nccn.org/professionals/physician_gls/f_guidelines.asp. Accessed 26 Aug 2012
  7. 7.
    Khatcheressian JL, Wolff AC, Smith TJ, Grunfeld E, Muss HB, Vogel VG, Halberg F, Somerfield MR, Davidson NE, American Society of Clinical Oncology (2006) American Society of Clinical Oncology 2006 update of the breast cancer follow-up and management guidelines in the adjuvant setting. J Clin Oncol 24:5091–5097. doi: 10.1200/JCO.2006.08.8575 PubMedCrossRefGoogle Scholar
  8. 8.
    Khatcheressian JL, Hurley P, Bantug E, Esserman LJ, Grunfeld E, Halberg F, Hantel A, Henry NL, Muss HB, Smith TJ, Vogel VG, Wolff AC, Somerfield MR, Davidson NE (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
  9. 9.
    Lash TL, Silliman RA (2001) Medical surveillance after breast cancer diagnosis. Med Care 39:945–955PubMedCrossRefGoogle Scholar
  10. 10.
    Keating NL, Landrum MB, Guadagnoli E, Winer EP, Ayanian JZ (2007) Surveillance testing among survivors of early-stage breast cancer. J Clin Oncol 25:1074–1081. doi: 10.1200/JCO.2006.08.6876 PubMedCrossRefGoogle Scholar
  11. 11.
    Doubeni CA, Field TS, Yood MU, Rolnick SJ, Quessenberry CP, Fouayzi H, Gurwitz JH, Wei F (2006) Patterns and predictors of mammography utilization among breast cancer survivors. Cancer 106:2482–2488PubMedCrossRefGoogle Scholar
  12. 12.
    Etim AE, Schellhase KG, Sparapani R, Nattinger AB (2006) Effect of model of care delivery on mammography use among elderly breast cancer survivors. Breast Cancer Res Treat 96:293–299. doi: 10.1007/s10549-005-9141-4 PubMedCrossRefGoogle Scholar
  13. 13.
    Field TS, Doubeni C, Fox MP, Buist DS, Wei F, Geiger AM, Quinn VP, Lash TL, Prout MN, Yood MU, Frost FJ, Silliman RA (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 PubMedCrossRefGoogle Scholar
  14. 14.
    Schapira MM, McAuliffe TL, Nattinger AB (2000) Underutilization of mammography in older breast cancer survivors. Med Care 38:281–289PubMedCrossRefGoogle Scholar
  15. 15.
    Lash TL, Fox MP, Buist DS, Wei F, Field TS, Frost FJ, Geiger AM, Quinn VP, Yood MU, Silliman RA (2007) Mammography surveillance and mortality in older breast cancer survivors. J Clin Oncol 25:3001–3006PubMedCrossRefGoogle Scholar
  16. 16.
    Enger SM, Thwin SS, Buist DS, Field T, Frost F, Geiger AM, Lash TL, Prout M, Yood MU, Wei F, Silliman RA (2006) Breast cancer treatment of older women in integrated health care settings. J Clin Oncol 24:4377–4383PubMedCrossRefGoogle Scholar
  17. 17.
    Geiger AM, Thwin SS, Lash TL, Buist DS, Prout MN, Wei F, Field TS, Yood MU, Frost FJ, Enger SM, Silliman RA (2007) Recurrences and second primary breast cancers in older women with initial early-stage disease. Cancer 109:966–974PubMedCrossRefGoogle Scholar
  18. 18.
    Yood MU, Owusu C, Buist DS, Geiger AM, Field TS, Thwin SS, Lash TL, Prout MN, Wei F, Quinn VP, Frost FJ, Silliman RA (2008) Mortality impact of less-than-standard therapy in older breast cancer patients. J Am Coll Surg 206:66–75PubMedCrossRefGoogle Scholar
  19. 19.
    Buist DS, Chubak J, Prout M, Yood MU, Bosco JL, Thwin SS, Gold HT, Owusu C, Field TS, Quinn VP, Wei F, Silliman RA (2009) Referral, receipt, and completion of chemotherapy in patients with early-stage breast cancer older than 65 years and at high risk of breast cancer recurrence. J Clin Oncol 27:4508–4514. doi: 10.1200/JCO.2008.18.3459 PubMedCrossRefGoogle Scholar
  20. 20.
    Wagner EH, Greene SM, Hart G, Field TS, Fletcher S, Geiger AM, Herrinton LJ, Hornbrook MC, Johnson CC, Mouchawar J, Rolnick SJ, Stevens VJ, Taplin SH, Tolsma D, Vogt TM (2005) Building a research consortium of large health systems: the Cancer Research Network. J Natl Cancer Inst Monogr 35:3–11Google Scholar
  21. 21.
    Fleming ID, Cooper JS, Henson DE, Hutter RVP, Kennedy BJ, Murphy GP et al (eds) (1997) AJCC cancer staging manual. Lippincott Williams & Wilkins, PhiladelphiaGoogle Scholar
  22. 22.
    Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40:373–383PubMedCrossRefGoogle Scholar
  23. 23.
    Houssami N, Abraham LA, Kerlikowske K, Buist DS, Irwig L, Lee J, Miglioretti DL (2013) Risk factors for second screen-detected or interval breast cancers in women with a personal history of breast cancer participating in mammography screening. Cancer Epidemiol Biomarkers Prev 22:946–961. doi: 10.1158/1055-9965.EPI-12-1208-T1055-9965.EPI-12-1208-T PubMedCrossRefGoogle Scholar
  24. 24.
    Houssami N, Abraham LA, Miglioretti DL, Sickles EA, Kerlikowske K, Buist DS, Geller BM, Muss HB, Irwig L (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 PubMedCrossRefGoogle Scholar
  25. 25.
    Buist DS, Abraham LA, Barlow WE, Krishnaraj A, Holdridge RC, Sickles EA, Carney PA, Kerlikowske K, Geller BM, For the Breast Cancer Surveillance Consortium (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 PubMedCrossRefGoogle Scholar
  26. 26.
    Swihart BJ, Caffo B, James BD, Strand M, Schwartz BS, Punjabi NM (2010) Lasagna plots: a saucy alternative to spaghetti plots. Epidemiology 21:621–625. doi: 10.1097/EDE.0b013e3181e5b06a PubMedCrossRefGoogle Scholar
  27. 27.
    Gao H, Buist DS, Lash TL, Bosco JL, Swihart B (2012) Lasagna plots made in different (statistical) ovens. Epidemiology 23:934. doi: 10.1097/EDE.0b013e31826d08c7 PubMedCrossRefGoogle Scholar
  28. 28.
    Therneau TM, Grambsch PM (2000) Modeling survival data: extending the Cox model. Springer, New YorkCrossRefGoogle Scholar
  29. 29.
    Humphrey L, Chan BKS, Detlefsen S, Helfand M (2002) Screening for breast cancer [internet]. In: Systematic evidence reviews. Database Agency for Healthcare Research and Quality. http://www.ncbi.nlm.nih.gov/books/NBK42742/. Accessed 3 Mar 2013
  30. 30.
    Nelson HD, Tyne K, Naik A, Bougatsos C, Chan B, Nygren P, L. H (2009) Screening for breast cancer: systematic evidence review update for the U.S. Preventive Services Task Force. Evidence review update no. 74. Rockville, MDGoogle Scholar
  31. 31.
    Lash TL, Clough-Gorr K, Silliman RA (2005) Reduced rates of cancer-related worries and mortality associated with guideline surveillance after breast cancer therapy. Breast Cancer Res Treat 89:61–67. doi: 10.1007/s10549-004-1472-z PubMedCrossRefGoogle Scholar
  32. 32.
    Grunfeld E, Noorani H, McGahan L, Paszat L, Coyle D, van Walraven C, Joyce J, Sawka C (2002) Surveillance mammography after treatment of primary breast cancer: a systematic review. Breast 11:228–235PubMedCrossRefGoogle Scholar
  33. 33.
    Koya DL, Chen JG, Smith TG, Moran WP (2011) Screening mammography use in Medicare beneficiaries reflects 4-year mortality risk. Am J Med 124(369):e361–368. doi: 10.1016/j.amjmed.2010.11.019 Google Scholar
  34. 34.
    Field TS, Bosco JL, Prout MN, Gold HT, Cutrona S, Pawloski PA, Yood MU, Quinn VP, Thwin SS, Silliman RA (2011) Age, comorbidity, and breast cancer severity: impact on receipt of definitive local therapy and rate of recurrence among older women with early-stage breast cancer. J Am Coll Surg 213:757–765. doi: 10.1016/j.jamcollsurg.2011.09.010 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Diana S. M. Buist
    • 1
    Email author
  • Jaclyn L. F. Bosco
    • 2
    • 3
  • Rebecca A. Silliman
    • 3
    • 4
    • 5
  • Heather Taffet Gold
    • 6
    • 7
  • Terry Field
    • 8
  • Marianne Ulcickas Yood
    • 5
    • 9
  • Virginia P. Quinn
    • 10
  • Marianne Prout
    • 3
    • 5
  • Timothy L. Lash
    • 11
  • The Breast Cancer Outcomes in Older Women (BOW) Investigators
  1. 1.Group Health Research InstituteSeattleUSA
  2. 2.Dana-Farber Cancer InstituteBostonUSA
  3. 3.Boston University School of MedicineBostonUSA
  4. 4.Boston Medical CenterBostonUSA
  5. 5.Boston University School of Public HealthBostonUSA
  6. 6.New York University School of MedicineNew YorkUSA
  7. 7.New York University Cancer InstituteNew YorkUSA
  8. 8.Meyers Primary Care Institute, A Joint Endeavor of the University of Massachusetts Medical SchoolFallon Community Health Plan, and Reliant Medical GroupWorcesterUSA
  9. 9.Henry Ford Health SystemDetroitUSA
  10. 10.Kaiser Permanente Southern CaliforniaPasadenaUSA
  11. 11.Rollins School of Public HealthEmory UniversityAtlantaUSA

Personalised recommendations