Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Epidemiology

Long-term trends in incidence, characteristics and prognosis of screen-detected and interval cancers in women participating in the Dutch breast cancer screening programme

Abstract

Background

No studies are available in which changes over time in characteristics and prognosis of patients with interval breast cancers (ICs) and screen-detected breast cancers (SDCs) have been compared. The aim was to study these trends between 1995 and 2018.

Methods

All women with invasive SDCs (N = 4290) and ICs (N = 1352), diagnosed in a southern mammography screening region in the Netherlands, were included and followed until date of death or 31 December 2022.

Results

The 5-year overall survival rate of women with SDCs increased from 91.4% for those diagnosed in 1995–1999 to 95.0% for those diagnosed in 2013–2018 (P < 0.001), and from 74.8 to 91.6% (P < 0.001) in the same periods for those with ICs. A similar trend was observed for the 10-year survival rates. After adjustment for changes in tumour characteristics, the hazard ratio (HR) for overall survival was 0.47 (95% confidence interval (CI): 0.38–0.59) for women with SDCs diagnosed in the period 2013–2018, compared to the women diagnosed in the period 1995–1999. For the women with ICs this HR was 0.27 (95% CI: 0.19–0.40).

Conclusion

The prognosis of women with ICs has improved rapidly since 1995 and is now almost similar to that of women with SDCs.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Cancer detection rate.
Fig. 2: Overall survival probability according to period of diagnosis.

Similar content being viewed by others

Data availability

All data supporting the findings in this study are presented in the manuscript and the supplementary information, and additional raw data can be made available by the corresponding author upon reasonable request.

References

  1. Peairs KS, Choi Y, Stewart RW. Screening for breast cancer. Semin Oncol. 2017;44:60–72.

    Article  PubMed  Google Scholar 

  2. IKNL. NKR Cijfers. Available from: https://iknl.nl/nkr-cijfers. Accessed on: 12-03-2022.

  3. Myers ER, Moorman P, Gierisch JM, Havrilesky LJ, Grimm LJ, Ghate S, et al. Benefits and harms of breast cancer screening: a systematic review. JAMA. 2015;314:1615–34.

    Article  CAS  PubMed  Google Scholar 

  4. Zielonke N, Gini A, Jansen EEL, Anttila A, Segnan N, Ponti A, et al. Evidence for reducing cancer-specific mortality due to screening for breast cancer in Europe: a systematic review. Eur J Cancer. 2020;127:191–206.

    Article  PubMed  Google Scholar 

  5. De Munck L, De Bock GH, Otter R, Reiding D, Broeders MJM, Willemse PHB, et al. Digital vs screen-film mammography in population-based breast cancer screening: performance indicators and tumour characteristics of screen-detected and interval cancers. Br J Cancer. 2016;115:517.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Van Luijt PA, Fracheboud J, Heijnsdijk EAM, Den Heeten GJ, De Koning HJ. Nation-wide data on screening performance during the transition to digital mammography: Observations in 6 million screens. Eur J Cancer. 2013;49:3517–25.

    Article  PubMed  Google Scholar 

  7. Nederend J, Duijm LEM, Louwman MWJ, Groenewoud JH, Donkers-Van Rossum AB, Voogd AC. Impact of transition from analog screening mammography to digital screening mammography on screening outcome in The Netherlands: a population-based study. Ann Oncol. 2012;23:3098–103.

    Article  CAS  PubMed  Google Scholar 

  8. van der Meer DJ, Kramer I, van Maaren MC, van Diest PJ, Linn SC, Maduro JH, et al. Comprehensive trends in incidence, treatment, survival and mortality of first primary invasive breast cancer stratified by age, stage and receptor subtype in the Netherlands between 1989 and 2017. Int J Cancer. 2021;148:2289–303.

    Article  PubMed  Google Scholar 

  9. Vugts G, Maaskant-Braat AJG, Nieuwenhuijzen GAP, Roumen RMH, Luiten EJT, Voogd AC. Patterns of care in the administration of neo-adjuvant chemotherapy for breast cancer. a population-based study. Breast J. 2016;22:316–21.

    Article  CAS  PubMed  Google Scholar 

  10. Berry DA, Cronin KA, Plevritis SK, Fryback DG, Clarke L, Zelen M, et al. Effect of screening and adjuvant therapy on mortality from breast cancer. N. Engl J Med. 2005;353:1784–92.

    Article  CAS  PubMed  Google Scholar 

  11. Kalager M, Zelen M, Langmark F, Adami HO. Effect of screening mammography on breast-cancer mortality in Norway. N Engl J Med. 2010;363:1203–10.

    Article  CAS  PubMed  Google Scholar 

  12. Grassmann F, He W, Eriksson M, Gabrielson M, Hall P, Czene K. Interval breast cancer is associated with other types of tumors. Nat Commun. 2019;10:4648.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  13. Timmermans L, De Brabander I, Van Damme N, Bleyen L, Martens P, Van Herck K, et al. Tumour characteristics of screen-detected and interval cancers in the flemish breast cancer screening programme: a mammographic breast density study. Maturitas. 2022;158:55–60.

    Article  PubMed  Google Scholar 

  14. Ernst MF, Voogd AC, Coebergh JWW, Roukema JA. Breast carcinoma diagnosis, treatment, and prognosis before and after the introduction of mass mammographic screening. Cancer. 2004;100:1337–44.

    Article  PubMed  Google Scholar 

  15. Rijksinstituut voor Volksgezonheid en Milieu. Bevolkingsonderzoek borstkanker. Available from: https://www.rivm.nl/bevolkingsonderzoek-borstkanker. Accessed on: 12-06-2022.

  16. Weber RJP, van Bommel RMG, Louwman MW, Nederend J, Voogd AC, Jansen FH, et al. Characteristics and prognosis of interval cancers after biennial screen-film or full-field digital screening mammography. Breast Cancer Res Treat. 2016;158:471–83.

    Article  PubMed  Google Scholar 

  17. Rakha EA, El-Sayed ME, Lee AHS, Elston CW, Grainge MJ, Hodi Z, et al. Prognostic significance of Nottingham histologic grade in invasive breast carcinoma. J Clin Oncol: Off J Am Soc Clin Oncol. 2008;26:3153–8.

    Article  Google Scholar 

  18. American College of Radiology. Illustrated Breast Imaging Reporting and Data System (BI-RADS). 3rd edn. Reston, VA, USA, 1998.

  19. American College of Radiology. Breast Imaging Reporting and Data System (BI-RADS). 4th edn. Reston, VA, USA, 2003.

  20. American College of Radiology, BI-RADS Committee. ACR BI-RADS atlas: breast imaging reporting and data system. 5th edn. Reston, VA, USA, 2013.

  21. van Buuren S, Groothuis-Oudshoorn K. Mice: multivariate imputation by chained equations in R. J Stat Softw. 2011;45:1–67.

    Article  Google Scholar 

  22. McNeish D. Missing data methods for arbitrary missingness with small samples. J Appl Stat. 2016;44:24–39.

    Article  MathSciNet  Google Scholar 

  23. Bellio G, Marion R, Giudici F, Kus S, Tonutti M, Zanconati F, et al. Interval breast cancer versus screen-detected cancer: comparison of clinicopathologic characteristics in a single-center analysis. Clin Breast Cancer. 2017;17:564–71.

    Article  PubMed  Google Scholar 

  24. Domingo L, Blanch J, Servitja S, Corominas JM, Murta-Nascimento C, Rueda A, et al. Aggressiveness features and outcomes of true interval cancers: comparison between screen-detected and symptom-detected cancers. Eur J Cancer Prev. 2013;22:21–8.

    Article  PubMed  Google Scholar 

  25. Weber RJP, van Bommel RMG, Setz-Pels W, Voogd AC, Klompenhouwer EG, Louwman MW, et al. Type and extent of surgery for screen-detected and interval cancers at blinded versus nonblinded double-reading in a population-based screening mammography program. Ann Surg Oncol. 2016;23:3822–30.

    Article  PubMed  Google Scholar 

  26. Niraula S, Biswanger N, Hu P, Lambert P, Decker K. Incidence, characteristics, and outcomes of interval breast cancers compared with screening-detected breast cancers. JAMA Netw Open. 2020;3:e2018179.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Hofvind S, Holen Å, Román M, Sebuødegård S, Puig-Vives M, Akslen L. Mode of detection: an independent prognostic factor for women with breast cancer. J Med Screen. 2016;23:89–97.

    Article  PubMed  Google Scholar 

  28. De Munck L, Schaapveld M, Siesling S, Wesseling J, Voogd AC, Tjan-Heijnen VCG, et al. Implementation of trastuzumab in conjunction with adjuvant chemotherapy in the treatment of non-metastatic breast cancer in the Netherlands. Breast Cancer Res Treat. 2011;129:229–33.

    Article  CAS  PubMed  Google Scholar 

  29. Beek MA, Verheuvel NC, Luiten EJT, Klompenhouwer EG, Rutten HJT, Roumen RMH, et al. Two decades of axillary management in breast cancer. Br J Surg. 2015;102:1658–64.

    Article  CAS  PubMed  Google Scholar 

  30. Blok EJ, Kroep JR, Kranenbarg EMK, Duijm-De Carpentier M, Putter H, Van Den Bosch J, et al. Optimal duration of extended adjuvant endocrine therapy for early breast cancer; results of the IDEAL trial (BOOG 2006-05). J Natl Cancer Inst. 2018;110:40–8.

    Article  CAS  Google Scholar 

  31. Derks MGM, Bastiaannet E, van de Water W, de Glas NA, Seynaeve C, Putter H, et al. Impact of age on breast cancer mortality and competing causes of death at 10 years follow-up in the adjuvant TEAM trial. Eur J Cancer. 2018;99:1–8.

    Article  CAS  PubMed  Google Scholar 

  32. Long H, Brooks JM, Harvie M, Maxwell A, French DP. How do women experience a false-positive test result from breast screening? A systematic review and thematic synthesis of qualitative studies. Br J Cancer. 2019;121:351–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Nelson HD, Pappas M, Cantor A, Griffin J, Daeges M, Humphrey L. Harms of breast cancer screening: systematic review to update the 2009 U.S. preventive services task force recommendation. Ann Intern Med. 2016;164:256–67.

    Article  PubMed  Google Scholar 

  34. Bolejko A, Zackrisson S, Hagell P, Wann-Hansson C. A roller coaster of emotions and sense-coping with the perceived psychosocial consequences of a false-positive screening mammography. J Clin Nurs. 2014;23:2053–62.

    Article  PubMed  Google Scholar 

  35. Dejean D, Krahn H, Giacomini M, Zierler A, Dhalla I, Sikich N, et al. Women’s experiences of inaccurate breast cancer screening results: a systematic review and qualitative meta-synthesis. Ont Health Technol Assess Ser. 2016;16:1.

    Google Scholar 

  36. Houssami N, Zackrisson S, Blazek K, Hunter K, Bernardi D, Lång K, et al. Meta-analysis of prospective studies evaluating breast cancer detection and interval cancer rates for digital breast tomosynthesis versus mammography population screening. Eur J Cancer (Oxf, Engl: 1990). 2021;148:14–23.

    Article  Google Scholar 

  37. Bakker MF, de Lange SV, Pijnappel RM, Mann RM, Peeters PHM, Monninkhof EM, et al. Supplemental MRI screening for women with extremely dense breast tissue. N Engl J Med. 2019;381:2091–102.

    Article  PubMed  Google Scholar 

  38. Allweis TM, Hermann N, Berenstein-Molho R, Guindy M. Personalized screening for breast cancer: rationale, present practices, and future directions. Ann Surg Oncol. 2021;28:4306–17.

    Article  PubMed  Google Scholar 

  39. Saccarelli CR, Bitencourt AGV, Morris EA. Is it the era for personalized screening? Radiol Clin North Am. 2021;59:129–38.

    Article  PubMed  Google Scholar 

  40. Geertse TD, van der Waal D, Vreuls W, Tetteroo E, Duijm LEM, Pijnappel RM, et al. The dilemma of recalling well-circumscribed masses in a screening population: A narrative literature review and exploration of Dutch screening practice. Breast (Edinb, Scotl). 2023;69:431–40.

    Article  Google Scholar 

  41. Mook S, Van ’T Veer LJ, Rutgers EJ, Ravdin PM, Van De Velde AO, Van Leeuwen FE, et al. Independent prognostic value of screen detection in invasive breast cancer. J Natl Cancer Inst. 2011;103:585–97.

    Article  PubMed  Google Scholar 

  42. Duffy SW, Tabár L, Yen AMF, Dean PB, Smith RA, Jonsson H, et al. Beneficial effect of consecutive screening mammography examinations on mortality from breast cancer: a prospective study. Radiology. 2021;299:541–7.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

Study design: LEMD and ACV. Performed the research and collected data: LEMD, DEV and ACV. Analyzed the data: DEV, LEMD and ACV. Manuscript drafting: DEV, ACV and LEM. Provided discussion, critical feedback and manuscript editing: ACV, LEM, MJCS, RJS, VCGTH, WV, LJAS.

Corresponding author

Correspondence to Adri C. Voogd.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

ten Velde, D.E., Duijm, L.E.M., van der Sangen, M.J.C. et al. Long-term trends in incidence, characteristics and prognosis of screen-detected and interval cancers in women participating in the Dutch breast cancer screening programme. Br J Cancer (2024). https://doi.org/10.1038/s41416-024-02633-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41416-024-02633-7

Search

Quick links