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Breast Cancer Research and Treatment

, Volume 166, Issue 3, pp 843–854 | Cite as

Trends in stage-specific breast cancer incidence in New South Wales, Australia: insights into the effects of 25 years of screening mammography

  • Gemma JacklynEmail author
  • Kevin McGeechan
  • Les Irwig
  • Nehmat Houssami
  • Stephen Morrell
  • Katy Bell
  • Alexandra Barratt
Epidemiology

Abstract

Purpose

Screening mammography aims to improve breast cancer (BC) prognosis by increasing the incidence of early-stage tumours in order to decrease the incidence of late-stage cancer, but no reports have investigated these potential effects in an Australian population. Therefore we aimed to identify temporal trends in stage-specific BC in New South Wales (NSW), Australia, between 1972 and 2012.

Methods

An observational study of women who received a diagnosis of BC from 1972–2012 as recorded in the NSW Cancer Registry, a population-based registry with almost complete coverage and high rates of histological verification. We analysed trends in stage-specific incidence before screening and compared them to periods after screening began. Our primary group of interest was women in the target age range of 50–69 years, though trends in women outside the target age were also assessed.

Results

Screening was not associated with lower incidence of late-stage BC at diagnosis. Incidence for all stages remained higher than prescreening levels. In women aged 50–69 years, the incidence of carcinoma in situ (CIS), localised and regional BC has more than doubled compared to the prescreening era, with incidence rate ratios ranging from 2.0 for regional (95% CI 1.95–2.13) to 121.8 for CIS (95% CI 82.58–179.72). Before the introduction of screening, there was a downward trend in distant metastatic BC incidence, and after the introduction of screening there was an increase (IRR 1.8; 95% CI 1.62–2.00). In women too young to screen the incidence of late-stage BC at diagnosis also increased, whereas localised disease was stable.

Conclusions

The incidence of all stages of BC has increased over the past 40 years, with the greatest rise seen during the established screening period for women aged 50–69 years. Our findings suggest that some of the expected benefits of screening may not have been realised and are consistent with overdiagnosis.

Keywords

Breast neoplasms Mass screening Mammography Epidemiology Medical overuse 

Abbreviations

BC

Breast cancer

CIS

Carcinoma in situ

HRT

Hormone replacement therapy

IR

Incidence rates

IRR

Incidence rate ratios

IRD

Incidence rate differences

MBS

Medicare benefits schedule

NSW

New South Wales

NSWCR

New South Wales Cancer Registry

SNB

Sentinel node biopsy

Notes

Acknowledgements

This work was supported by grants from the National Health and Medical Research Centre, Australia. A postgraduate scholarship (Grant No 1074626) was awarded to GJ and a Centre for Research Excellence award (Grant No 1104136) was awarded to AB. Incidence data were supplied by the NSW Central Cancer Registry, which is managed and operated by The Cancer Council NSW under contract to the NSW Health Department.

Compliance with ethical standards

Conflicts of interest

All authors declare that they do not have any conflicts of interest to report.

Ethical approval

Our research protocol was approved by the research ethics board of the NSW Population & Health Services Research Ethics Committee (Cancer Institute NSW reference number: LNR 2014/07/032).

References

  1. 1.
    Cole P, Morrison AS (1980) Basic issues in population screening for cancer. J Natl Cancer Inst 64(5):1263–1272PubMedGoogle Scholar
  2. 2.
    Morrison AS (1992) Screening in chronic disease. Monographs in epidemiology and biostatistics (Book 19), 2nd edn. Oxford University Press, New YorkGoogle Scholar
  3. 3.
    Haybittle J, Blamey R, Elston C, Johnson J, Doyle P, Campbell F, Nicholson R, Griffiths K (1982) A prognostic index in primary breast cancer. Br J Cancer 45(3):361CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Fitzgibbons PL, Page DL, Weaver D, Thor AD, Allred DC, Clark GM, Ruby SG, O’Malley F, Simpson JF, Connolly JL (2000) Prognostic factors in breast cancer: College of American Pathologists consensus statement 1999. Arch Pathol Lab Med 124(7):966–978PubMedGoogle Scholar
  5. 5.
    Bleyer A, Welch HG (2012) Effect of three decades of screening mammography on breast-cancer incidence. N Engl J Med 367(21):1998–2005CrossRefPubMedGoogle Scholar
  6. 6.
    Buiatti E, Barchielli A, Bartolacci S, Federico M, De Lisi V, Bucchi L, Ferretti S, Paci E, Segnan N, Tumino R (2003) The impact of organised screening programmes on the stage-specific incidence of breast cancer in some Italian areas. Eur J Cancer 39(12):1776–1782CrossRefPubMedGoogle Scholar
  7. 7.
    Esserman L, Shieh Y, Thompson I (2009) Rethinking screening for breast cancer and prostate cancer. JAMA 302(15):1685–1692CrossRefPubMedGoogle Scholar
  8. 8.
    Hofvind S, Lee CI, Elmore JG (2012) Stage-specific breast cancer incidence rates among participants and non-participants of a population-based mammographic screening program. Breast Cancer Res Treat 135(1):291–299CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Kalager M, Adami H-O, Bretthauer M, Tamimi RM (2012) Overdiagnosis of invasive breast cancer due to mammography screening: results from the Norwegian screening program. Ann Intern Med 156(7):491–499CrossRefPubMedGoogle Scholar
  10. 10.
    Lousdal ML, Kristiansen IS, Møller B, Støvring H (2014) Trends in breast cancer stage distribution before, during and after introduction of a screening programme in Norway. Eur J Public Health 24(6):1017–1022CrossRefPubMedGoogle Scholar
  11. 11.
    Lousdal ML, Kristiansen IS, Møller B, Støvring H (2016) Effect of organised mammography screening on stage-specific incidence in Norway: population study. Br J Cancer 114(5):590–596CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    McCann J, Stockton D, Day N (1998) Breast cancer in East Anglia: the impact of the breast screening programme on stage at diagnosis. J Med Screen 5(1):42–48CrossRefPubMedGoogle Scholar
  13. 13.
    Australian Institute of Health and Welfare (2017) Australian Cancer Incidence and Mortality (ACIM) books: Breast cancer. Available from: AIHW. www.aihw.gov.au/acim-books. Accessed 7 June 2017
  14. 14.
    Osborn M, Armstrong B, Kricker A, Coates M (1999) Current recording and registration practices for carcinoma in situ (CIS) of the breast in Australasian State and Territory cancer registries. NHMRC National Breast Cancer Centre, SydneyGoogle Scholar
  15. 15.
    Australian Bureau of Statistics (2014) Australian Historical Population Statistics, 2014. Population Age-Sex Structure. Available from: http://www.abs.gov.au/ausstats/abs@.nsf/0/632CDC28637CF57ECA256F1F0080EBCC?Opendocument. Accessed 9 Feb 2017
  16. 16.
    Young JL Jr, Roffers SD, Ries LAG, Fritz AG, Hurlbut AA (eds) (2001) SEER summary staging manual—2000: codes and coding instructions. National Cancer Institute, BethesdaGoogle Scholar
  17. 17.
    Department of Health and Ageing (2009) BreastScreen Australia evaluation. Screening Monograph No.1/2009. Evaluation final report. Canberra, AustraliaGoogle Scholar
  18. 18.
    Cancer Institute NSW (2006) Annual report 2005–2006. Cancer Institute NSW, SydneyGoogle Scholar
  19. 19.
    Australian Bureau of Statistics (2013) Which population to use for age standardisation? Australian Bureau of Statistics. Available from: http://www.abs.gov.au/ausstats/abs@.nsf/products/42479A8EF04E40EBCA257C430016EA3B?OpenDocument. Accessed 31 May 2017
  20. 20.
    SAS Institute Inc (2011) SAS version 9.4 of the SAS System for Windows. SAS Institute Inc, CaryGoogle Scholar
  21. 21.
    Esteve J, Benhamou E, Raymond L (1994) Statistical methods in cancer research. Volume IV. Descriptive epidemiology. IARC Sci Publ 1(128):302Google Scholar
  22. 22.
    Baum M, Houghton J (1999) Contribution of randomised controlled trials to understanding and management of early breast cancer. BMJ 319(7209):568CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Verghese A, Brady E, Kapur CC, Horwitz RI (2011) The bedside evaluation: ritual and reason. Ann Intern Med 155(8):550–553CrossRefPubMedGoogle Scholar
  24. 24.
    Amir E, Clemons M (2009) Should a biopsy be recommended to confirm metastatic disease in women with breast cancer? Lancet Oncol 10(10):933–935CrossRefPubMedGoogle Scholar
  25. 25.
    Bouchardy C, Rapiti E, Blagojevic S, Vlastos A-T, Vlastos G (2007) Older female cancer patients: importance, causes, and consequences of undertreatment. J Clin Oncol 25(14):1858–1869CrossRefPubMedGoogle Scholar
  26. 26.
    Levi F, Te V-C, Randimbison L, La Vecchia C (1997) Trends of in situ carcinoma of the breast in Vaud, Switzerland. Eur J Cancer 33(6):903–906CrossRefPubMedGoogle Scholar
  27. 27.
    Zahl P, Jørgensen KJ, Gøtzsche P (2013) Overestimated lead times in cancer screening has led to substantial underestimation of overdiagnosis. Br J Cancer 109(7):2014–2019CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Chlebowski RT, Hendrix SL, Langer RD, Stefanick ML, Gass M, Lane D, Rodabough RJ, Gilligan MA, Cyr MG, Thomson CA (2003) Influence of estrogen plus progestin on breast cancer and mammography in healthy postmenopausal women: the Women’s Health Initiative Randomized Trial. JAMA 289(24):3243–3253CrossRefPubMedGoogle Scholar
  29. 29.
    Canfell K, Banks E, Moa AM, Beral V (2008) Decrease in breast cancer incidence following a rapid fall in use of hormone replacement therapy in Australia. Med J Aust 188(11):641–644PubMedGoogle Scholar
  30. 30.
    Canfell K, Banks E, Clements M, Kang YJ, Moa A, Armstrong B, Beral V (2009) Sustained lower rates of HRT prescribing and breast cancer incidence in Australia since 2003. Breast Cancer Res Treat 117(3):671–673CrossRefPubMedGoogle Scholar
  31. 31.
    Australian Bureau of Statistics (1996) 1995 National Nutrition Survey. Basic Confidentialised Unit Record File (CURF), CD-ROM. Findings based on use of ABS Microdata. Canberra, AustraliaGoogle Scholar
  32. 32.
    Australian Bureau of Statistics (2002) 2001 National Health Survey. Expanded Confidentialised Unit Record File (CURF), Remote Access Data Laboratory (RADL). Findings based on use of ABS Microdata. Canberra, AustraliaGoogle Scholar
  33. 33.
    Writing Group for the Women’s Health Initiative Investigators (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women’s Health Initiative randomized controlled trial. JAMA 288(3):321–333CrossRefGoogle Scholar
  34. 34.
    Ravdin PM, Cronin KA, Howlader N, Berg CD, Chlebowski RT, Feuer EJ, Edwards BK, Berry DA (2007) The decrease in breast-cancer incidence in 2003 in the United States. N Engl J Med 356(16):1670–1674CrossRefPubMedGoogle Scholar
  35. 35.
    Chua B, Ung O, Taylor R, Bilous M, Salisbury E, Boyages J (2001) Treatment implications of a positive sentinel lymph node biopsy for patients with early-stage breast carcinoma. Cancer 92(7):1769–1774CrossRefPubMedGoogle Scholar
  36. 36.
    Ung OA (2004) Australasian experience and trials in sentinel lymph node biopsy: the RACS SNAC trial. Asian J Surg 27(4):284–290CrossRefPubMedGoogle Scholar
  37. 37.
    Morris T, Wetzig N, Sinclair S, Kollias J, Zorbas H (2012) Evaluation of implementation of sentinel node biopsy in Australia. ANZ J Surg 82(7–8):541–547CrossRefPubMedGoogle Scholar
  38. 38.
    Bilous M, Morey A, Armes J, Cummings M, Francis G (2006) Chromogenic in situ hybridisation testing for HER2 gene amplification in breast cancer produces highly reproducible results concordant with fluorescence in situ hybridisation and immunohistochemistry. Pathology (Phila) 38(2):120–124Google Scholar
  39. 39.
    Giuliano AE, Dale PS, Turner RR, Morton DL, Evans SW, Krasne DL (1995) Improved axillary staging of breast cancer with sentinel lymphadenectomy. Ann Surg 222(3):394CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Brennan M, Houssami N (2012) Evaluation of the evidence on staging imaging for detection of asymptomatic distant metastases in newly diagnosed breast cancer. Breast 21(2):112–123CrossRefPubMedGoogle Scholar
  41. 41.
    Munsell MF, Sprague BL, Berry DA, Chisholm G, Trentham-Dietz A (2014) Body mass index and breast cancer risk according to postmenopausal estrogen-progestin use and hormone receptor status. Epidemiol Rev 36(1):114–136CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Hunter DJ, Spiegelman D, Adami H-O, van den Brandt PA, Folsom AR, Goldbohm RA, Graham S, Howe GR, Kushi LH, Marshall JR, Miller AB, Speizer FE, Willett W, Wolk A, Yaun S-S (1997) Non-dietary factors as risk factors for breast cancer, and as effect modifiers of the association of fat intake and risk of breast cancer. Cancer Causes Control 8(1):49–56CrossRefPubMedGoogle Scholar
  43. 43.
    Ewertz M, Duffy SW, Adami HO, Kvåle G, Lund E, Meirik O, Mellemgaard A, Soini I, Tulinius H (1990) Age at first birth, parity and risk of breast cancer: a meta-analysis of 8 studies from the nordic countries. Int J Cancer 46(4):597–603CrossRefPubMedGoogle Scholar
  44. 44.
    Jørgensen K, Gøtzsche PC, Kalager M, Zahl P (2017) Breast cancer screening in Denmark: a cohort study of tumor size and overdiagnosis. Ann Intern Med 166(5):313–323CrossRefPubMedGoogle Scholar
  45. 45.
    Autier P (2016) Mammography screening effectiveness and overdiagnosis in the Netherlands. In: Paper presented at the 4th international conference on Preventing Overdiagnosis, Barcelona, Spain, 20–22 SeptGoogle Scholar
  46. 46.
    Harding C, Pompei F, Burmistrov D, Welch HG, Abebe R, Wilson R (2015) Breast cancer screening, incidence, and mortality across US counties. JAMA Intern Med 175(9):1483–1489CrossRefPubMedGoogle Scholar
  47. 47.
    Autier P, Boniol M, Middleton R, Doré J-F, Héry C, Zheng T, Gavin A (2011) Advanced breast cancer incidence following population-based mammographic screening. Ann Oncol 22(8):1726–1735CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    de Glas NA, de Craen AJ, Bastiaannet E, Op’t Land EG, Kiderlen M, van de Water W, Siesling S, Portielje JE, Schuttevaer HM, de Bock GTH (2014) Effect of implementation of the mass breast cancer screening programme in older women in the Netherlands: population based study. BMJ 349:g5410CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Hofvind S, Skaane P, Elmore JG, Sebuødegård S, Hoff SR, Lee CI (2014) Mammographic performance in a population-based screening program: before, during, and after the transition from screen-film to full-field digital mammography. Radiology 272(1):52–62CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Karssemeijer N, Bluekens AM, Beijerinck D, Deurenberg JJ, Beekman M, Visser R, Rv Engen, Bartels-Kortland A, Broeders MJ (2009) Breast cancer screening results 5 years after introduction of digital mammography in a population-based screening program. Radiology 253(2):353–358CrossRefPubMedGoogle Scholar
  51. 51.
    Weber RJ, Nederend J, Voogd AC, Strobbe LJ, Duijm LE (2015) Screening outcome and surgical treatment during and after the transition from screen-film to digital screening mammography in the south of The Netherlands. Int J Cancer 137(1):135–143CrossRefPubMedGoogle Scholar
  52. 52.
    Cancer Institute NSW (2016) Annual NSW cancer incidence and mortality data set, 2012. Cancer Registry NSW. Available at: http://www.statistics.cancerinstitute.org.au/trends_agegroup/trends_agegroup_mort_C50_NSW_extall_2.htm. Accessed 1 Aug 2017
  53. 53.
    Morrell S, Taylor R, Roder D, Dobson A (2012) Mammography screening and breast cancer mortality in Australia: an aggregate cohort study. J Med Screen 19(1):26–34CrossRefPubMedGoogle Scholar
  54. 54.
    Berry DA, Cronin KA, Plevritis SK, Fryback DG, Clarke L, Zelen M, Mandelblatt JS, Yakovlev AY, Habbema JDF, Feuer EJ (2005) Effect of screening and adjuvant therapy on mortality from breast cancer. N Engl J Med 353(17):1784–1792CrossRefPubMedGoogle Scholar
  55. 55.
    Independent UK Panel on Breast Cancer Screening (2012) The benefits and harms of breast cancer screening: an independent review. Lancet 380(9855):1778–1786CrossRefGoogle Scholar
  56. 56.
    Fisher B (1980) Laboratory and clinical research in breast cancer—a personal adventure: the David A. Karnofsky memorial lecture. Cancer Res 40(11):3863–3874PubMedGoogle Scholar
  57. 57.
    Halsted WS (1907) I. The results of radical operations for the cure of carcinoma of the breast. Ann Surg 46(1):1CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Welch HG, Gorski DH, Albertsen PC (2015) Trends in metastatic breast and prostate cancer—lessons in cancer dynamics. N Engl J Med 373:1685–1687CrossRefPubMedGoogle Scholar
  59. 59.
    Fisher B, Anderson S, Bryant J, Margolese RG, Deutsch M, Fisher ER, Jeong J-H, Wolmark N (2002) Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer. N Engl J Med 347(16):1233–1241CrossRefPubMedGoogle Scholar
  60. 60.
    Identifier NCT02926911, Comparison of operative to monitoring and endocrine therapy (COMET) trial for low risk DCIS (COMET), 2016 Sept 19 (2000) National Library of Medicine (US). Available at: https://clinicaltrials.gov/ct2/show/NCT02926911. Accessed 4 June 2017
  61. 61.
    Morrell S, Barratt A, Irwig L, Howard K, Biesheuvel C, Armstrong B (2010) Estimates of overdiagnosis of invasive breast cancer associated with screening mammography. Cancer Causes Control 21(2):275–282CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Sydney School of Public HealthThe University of SydneySydneyAustralia
  2. 2.School of Public Health and Community Medicine, Faculty of MedicineUniversity of New South WalesSydneyAustralia
  3. 3.Wiser Healthcare, Sydney School of Public HealthThe University of SydneySydneyAustralia

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