Skip to main content

Advertisement

Log in

Screen-detected versus interval cancers: Effect of imaging modality and breast density in the Flemish Breast Cancer Screening Programme

  • Breast
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

To investigate if direct radiography (DR) performs better than screen-film mammography (SF) and computed radiography (CR) in dense breasts in a decentralized organised Breast Cancer Screening Programme. To this end, screen-detected versus interval cancers were studied in different BI-RADS density classes for these imaging modalities.

Methods

The study cohort consisted of 351,532 women who participated in the Flemish Breast Cancer Screening Programme in 2009 and 2010. Information on screen-detected and interval cancers, breast density scores of radiologist second readers, and imaging modality was obtained by linkage of the databases of the Centre of Cancer Detection and the Belgian Cancer Registry.

Results

Overall, 67% of occurring breast cancers are screen detected and 33% are interval cancers, with DR performing better than SF and CR. The interval cancer rate increases gradually with breast density, regardless of modality. In the high-density class, the interval cancer rate exceeds the cancer detection rate for SF and CR, but not for DR.

Conclusions

DR is superior to SF and CR with respect to cancer detection rates for high-density breasts. To reduce the high interval cancer rate in dense breasts, use of an additional imaging technique in screening can be taken into consideration.

Key Points

Interval cancer rate increases gradually with breast density, regardless of modality.

Cancer detection rate in high-density breasts is superior in DR.

IC rate exceeds CDR for SF and CR in high-density breasts.

DR performs better in high-density breasts for third readings and false-positives.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Kankerregister, Breast cancer in females: comparison of age standardised incidence rates (WSR), 2008, fig 57. Kankerregister, Belgium. Available via www.kankerregister.org

  2. Vlaams agentschap zorg en gezondheid, Belgium. Available via www.zorg-en-gezondheid.be

  3. Timmermans L, De Hauwere A, Bacher K, Bosmans H, Lemmens K, Bleyen L, Van Limbergen E, Martens P, Van Steen A, Mortier M, Van Herck K, Thierens H (2014) Impact of the digitalisation of mammography on performance parameters and breast dose in the Flemish Breast Cancer Screening Programme. Eur Radiol 24:1808–1819

    Article  PubMed  Google Scholar 

  4. American college of Radiology (2003) Breast Imaging and Data Sytem Atlas, 4th edn. American College of Radiology, Reston, VA

    Google Scholar 

  5. McCormack VA, dos Santos Silva I (2006) Breast density and parenchymal patterns as markers of breast cancer risk: a meta-analysis. Cancer Epidemiol Biomarkers Prev 15:1159–1169

    Article  PubMed  Google Scholar 

  6. Boyd NF, Byng JW, Jong RA, Fishell EK, Little LE, Miller AB, Lockwood GA, Tritchler DL, Yaffe MJ (1995) Quantitative classification of mammographic densities and breast cancer risk: results from the Canadian National Breast Screening Study. J Natl Cancer Inst 87:670–675

    Article  CAS  PubMed  Google Scholar 

  7. Boyd NF, Lockwood GA, Martin LJ, Knight JA, Byng JW, Yaffe MJ, Tritchler DL (1998) Mammographic densities and breast cancer risk. Breast Dis 10:113–126

    Article  CAS  PubMed  Google Scholar 

  8. Byrne C, Schairer C, Wolfe J, Parekh N, Salane M, Brinton LA, Hoover R, Haile R (1995) Mammographic Features and Breast Cancer Risk: Effects With Time, Age, and Menopause Status. J Natl Cancer Inst 87:1622–1629

    Article  CAS  PubMed  Google Scholar 

  9. Kerlikowske K, Grady D, Barclay J, Sickles EA, Ernster V (1996) Effect of age, breast density, and family history on the sensitivity of first screening mammography. JAMA 276:33–38

    Article  CAS  PubMed  Google Scholar 

  10. Lehman CD, White E, Peacock S, Drucker MJ, Urban N (1999) Effect of age and breast density on screening mammograms with false-positive findings. AJR Am J Roentgenol 173:1651–1655

    Article  CAS  PubMed  Google Scholar 

  11. Osako T, Iwase T, Takahashi K, Iijima K, Miyagi Y, Nishimura S, Kasumi F (2007) Diagnostic mammography and ultrasonography for palpable and nonpalpable breast cancer in women aged 30 to 39 years. Breast Cancer 14:255–259

  12. Osako T, Takahashi K, Iwase T, Iijima K, Miyagi Y, Nishimura S, Kasumi F (2007). Diagnostic ultrasonography and mammography for invasive and noninvasive breast cancer in women aged 30 to 39 years. Breast Cancer 14:229–233

  13. Carney PA., Miglioretti DL, Yankaskas BC, Kerlikowske K, Rosenberg R, Rutter CM, Ballard-Barbash R (2003) Individual and combined effects of age, breast density, and hormone replacement therapy use on the accuracy of screening mammography. Ann Intern Med 138(1539-3704 (Electronic)):168–175

  14. Kavanagh AM, Byrnes GB, Nickson C, Cawson JN, Giles GG, Hopper JL, English DR (2008) Using mammographic density to improve breast cancer screening outcomes. Cancer Epidemiol Biomarkers Prev 17:2818–2824

  15. Perry N, Broeders M, de Wolf C, Törnberg S, Holland R, vonKarsa L (2006) European guidelines for quality assurance in breast cancer screening and diagnosis, 4th edn. European Communities, Luxemburg

    Google Scholar 

  16. Porter PL, El-astawissi AY, Mandelson MT, Lin MG, Khalid N, Watney EA, Cousens L, White D, Taplin S, White E (1999) Breast Tumor Characteristics as Predictors of Mammographic Detection : Comparison of Interval- and Screen-Detected Cancers screening is useful for detecting early Selection of Subjects. J Natl Cancer Inst 91:2020–2028

    Article  CAS  PubMed  Google Scholar 

  17. Al Mousa DS, Ryan EA, Mello-Thoms C, Brennan PC (2014) What effect does mammographic breast density have on lesion detection in digital mammography? Clin Radiol 69:333–341

    Article  Google Scholar 

  18. Pisano ED, Hendrick RE, Yaffe MJ, Baum JK, Acharyya S, Cormack JB, Hanna LA, Conant EF, Fajardo LL, Bassett LW, D'Orsi CJ, Jong RA, Rebner M, Tosteson AN, Gatsonis CA, DMIST Investigators Group (2008) Diagnostic accuracy of digital versus film mammography: exploratory analysis of selected population subgroups in DMIST. Radiology 246:376-83

  19. Wet van 13 december 2006 houdende de diverse bepalingen betreffende gezondheid. Federale Overheidsdienst Volksgezondheid, Veiligheid van de Voedselketen en Leefmilieu. Belgisch Staatsblad (publicatie 22 december 2006):73782-73814

  20. Beraadslaging nr. 14/115 van 16 december 2014 betreffende de uitwisseling van persoonsgegevens die de gezondheid betreffen door het centrum voor kankeropsporing, de stichting kankerregister en de verzekeringsinstellingen in het kader van het bevolkingsonderzoek naar borstkanker

  21. Skaane P, Skjennald A (2004) Screen-film mammography versus full-field digital mammography with soft-copy reading: randomized trial in a population-based screening program the Oslo II study. Radiology 232:197–204

    Article  PubMed  Google Scholar 

  22. Hambly NM, McNicholas MM, Phelan N, Hargaden GC, O'Doherty A, Flanagan FL (2009) Comparison of digital mammography and screen-film mammography in breast cancer screening: a review in the Irish breast screening program. AJR Am J Roentgenol 193:1010-1018

  23. Heddson B, Rönnow K, Olsson M, Miller D (2007) Digital versus screen-film mammography: a retrospective comparison in a population-based screening program. Eur J Radiol 64:419–425

    Article  PubMed  Google Scholar 

  24. Vigeland E, Klaasen H, Klingen T, Hofvind S, Skaane P (2008) Full-field digital mammography compared to screen film mammography in the prevalent round of a population-based screening programme: the Vestfold County Study. Eur Radiol 18:183-191

  25. Fischer U, Baum F, Obenauer S, Luftner-Nagel S, von Heyden D, Vosshenrich R, Grabbe E (2002) Comparative study in patients with microcalcifications: full-field digital mammography vs screen-film mammography. Eur Radiol 12:2679-2683

  26. Del Turco MR, Mantellini P, Ciatto S, Bonardi R, Martinelli F, Lazzari B, Houssami N (2007) Full-field digital versus screen-film mammography: Comparative accuracy in concurrent screening cohorts. Am J Roentgenol 189:860–866

    Article  Google Scholar 

  27. Yang WT, Lai CJ, Whitman GJ, Murphy WA Jr, Dryden MJ, Kushwaha AC, Sahin AA, Johnston D, Dempsey PJ, Shaw CC (2006) Comparison of full-field digital mammography and screen-film mammography for detection and characterization of simulated small masses. AJR Am J Roentgenol 187:W576–W581

    Article  PubMed  PubMed Central  Google Scholar 

  28. Hermann KP, Obenauer S, Funke M, Grabbe EH (2002) Magnification mammography: a comparison of full-field digital mammography and screen-film mammography for the detection of simulated small masses and microcalcifications. Eur Radiol 12:2188–2191

    Article  PubMed  Google Scholar 

  29. Fischmann A, Siegmann KC, Wersebe A, Claussen CD, Müller-Schimpfle M (2005) Comparison of full-field digital mammography and film-screen mammography: image quality and lesion detection. Br J Radiol 78:312–315

    Article  CAS  PubMed  Google Scholar 

  30. Skaane P, Hofvind S, Skjennald A (2007) Randomized trial of screen-film versus full-field digital mammography with soft-copy reading in population-based screening program: follow-up and final results of Oslo II study. Radiology 244:708–717

    Article  PubMed  Google Scholar 

  31. Skaane P, Balleyguier C, Diekmann F, Diekmann S, Piguet JC, Young K, Niklason LT (2005) Breast lesion detection and classification: comparison of screen-film mammography and full-field digital mammography with soft-copy reading--observer performance study. Radiology 237:37–44

    Article  PubMed  Google Scholar 

  32. Lewin JM, D'Orsi CJ, Hendrick RE, Moss LJ, Isaacs PK, Karellas A, Cutter GR (2002) Clinical comparison of full-field digital mammography and screen-film mammography for detection of breast cancer. AJR Am J Roentgenol 179:671–677

    Article  PubMed  Google Scholar 

  33. Bluekens AM, Karssemeijer N, Beijerinck D, Deurenberg JJ, van Engen RE, Broeders MJ, den Heeten GJ (2010) Consequences of digital mammography in population-based breast cancer screening: initial changes and long-term impact on referral rates. Eur Radiol 20:2067–2073

    Article  PubMed  PubMed Central  Google Scholar 

  34. Bluekens AMJ, Holland R, Karssemeijer N, Broeders MJM, den Heeten GJ (2012) Comparison of digital screening mammography and screen-film mammography in the early detection of clinically relevant cancers: a multicenter study. Radiology 265:707–714

    Article  PubMed  Google Scholar 

  35. Sala M, Comas M, Macia F, Martinez J, Casamitjana M, Castells X (2009) Implementation of digital mammography in a populationbased breast cancer screening programme: effect of screening round on recall rate and cancer detection. Radiology 252:31–39

    Article  PubMed  Google Scholar 

  36. Van Ongeval C, Van Steen A, Vande Putte G, Zanca F, Bosmans H, Marchal G, Van Limbergen E (2010) Does digital mammography in a decentralized breast cancer screening programme lead to screening performance parameters comparable with film-screen mammography? Eur Radiol 20:2307–2314

    Article  PubMed  Google Scholar 

  37. Chiarelli AM, Edwards SA, Prummel MV, Muradali D, Majpruz V, Done SJ, Brown P, Shumak RS, Yaffe MJ (2013) Digital compared with screen- film mammography: Performance Measures in concurrent cohorts within an organized breast screening program. Radiology 268:684–693

    Article  PubMed  Google Scholar 

  38. Harvey J, Bovbjerg VE (2004) Quantitative assessment of mammographic breast density: relationship with breast cancer risk. Radiology 230:29–41

    Article  PubMed  Google Scholar 

  39. Olsen AH, Bihrmann K, Jensen MB, Vejborg I, Lynge E (2009) Breast density and outcome of mammography screening: a cohort study. Br J Cancer 100:1205–1208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Mandelson MT, Oestreicher N, Porter PL, White D, Finder CA, Taplin SH, White E (2000) Breast Density as a Predictor of Mammographic Detection: Comparison of Interval- and Screen-Detected Cancers. J Natl Cancer Inst 92:1081–1087

    Article  CAS  PubMed  Google Scholar 

  41. Ciatto S, Visioli C, Paci E, Zappa M (2004) Breast density as a determinant of interval cancer at mammographic screening. Br J Cancer 90:393–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Chiarelli AM, Kirsh VA, Klar NS, Shumak R, Jong R, Fishell E, … Boyd NF (2006) Influence of patterns of hormone replacement therapy use and mammographic density on breast cancer detection. Cancer Epidemiol Biomarkers Prev 15:1856–1862

  43. Weigel S, Heindel W, Heindrich J, Hense H-W, Heidinger O (2016) Digital mammography screening: sensitivity of the programme dependent on breast density. Eur Radiol

  44. Kerlikowske K, Hubbard RA, Miglioretti DL, Geller BM, Yankaskas BC, Lehman CD, Taplin SH, Sickles EA, Breast Cancer Surveillance Consortium (2011) Comparative effectiveness of digital versus film-screen mammography in community practice in the United States: a cohort study. Ann Intern Med 155:493–502

    Article  PubMed  PubMed Central  Google Scholar 

  45. Pisano ED, Gatsonis C, Hendrick E, Yaffe M, Baum JK, Acharyya S, Rebner M (2005) Diagnostic performance of digital versus film mammography for breast-cancer screening. N Engl J Med 353:1773–83

  46. Pisano ED, Hendrick RE, Yaffe MJ, Baum JK, Acharyya S, Cormack JB, Gatsonis C (2008) Diagnostic accuracy of digital versus film mammography: exploratory analysis of selected population subgroups in DMIST. Radiology 246:376–383

  47. Ciatto S, Houssami N, Bernardi D, Caumo F, Pellegrini M, Brunelli S, Tuttobene P, Bricolo P, Fantò C, Valentini M, Montemezzi S, Macaskill P (2013) Integration of 3D digital mammography with tomosynthesis for population breast-cancer screening (STORM): a prospective comparison study. Lancet Oncol 14:583–589

    Article  PubMed  Google Scholar 

  48. Lee CH, Dershaw DD, Kopans D, Evans P, Monsees B, Monticciolo D, Brenner RJ, Bassett L, Berg W, Feig S, Hendrick E, Mendelson E, D'Orsi C, Sickles E, Burhenne LW (2010) Breast cancer screening with imaging: recommendations from the Society of Breast Imaging and the ACR on the use of mammography, breast MRI, breast ultrasound, and other technologies for the detection of clinically occult breast cancer. J Am Coll Radiol 7:18–27

    Article  PubMed  Google Scholar 

  49. Schousboe JT, Kerlikowske K, Loh A, Cummings SR (2011) Personalizing mammography by breast density and other risk factors for breast cancer: analysis of health benefits and cost-effectiveness. Ann Intern Med 155:10–20

    Article  PubMed  PubMed Central  Google Scholar 

  50. Price ER, Hargreaves J, Lipson JA, Sickles EA, Brenner RJ, Lindfors KK, Ikeda DM (2013) The California breast density information group: a collaborative response to the issues of breast density, breast cancer risk, and breast density notification legislation. Radiology 269:887–892

  51. Evans DGR, Warwick J, Astley SM, Stavrinos P, Sahin S, Ingham S, McBurney H, Eckersley B, Harvie M, Wilson M, Beetles U, Warren R, Hufton A, Sergeant JC, Newman WG, Buchan I, Cuzick J, Howell A (2012) Assessing Individual Breast Cancer Risk within the U.K. National Health Service Breast Screening Program: A New Paradigm for Cancer Prevention. Cancer Prev Res 5:943–951

    Article  Google Scholar 

Download references

Acknowledgements

We wish to thank all members of the research working group and the general working group of the Breast Cancer Screening of the Flemish Government for their contribution. Special thanks go to the colleagues of the physical-technical quality assurance of LUCMFR, VUB and Controlatom. We also express our gratitude to VolparaSolutions® for use of the scientific version of VolparaDensity® software. Finally, last but not least, we wish to thank the Centres for Cancer Detection and the National Cancer Registry.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lore Timmermans.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Prof. Hubert Thierens

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Funding

The authors state that this work has not received any funding.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Ethical approval

Institutional Review Board approval was not required because the data were collected routinely in the context of a screening programme.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Women who participated in the screening programme gave their consent for collection of the data.

This consent includes allowing the use of the data for several projects, as for this evaluation.

Methodology

• retrospective

• observational

• multicentre study

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Timmermans, L., Bleyen, L., Bacher, K. et al. Screen-detected versus interval cancers: Effect of imaging modality and breast density in the Flemish Breast Cancer Screening Programme. Eur Radiol 27, 3810–3819 (2017). https://doi.org/10.1007/s00330-017-4757-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-017-4757-4

Keywords

Navigation