Delayed breast cancer diagnosis after repeated recall at biennial screening mammography: an observational follow-up study from the Netherlands



Delay in detection of breast cancer may worsen tumour characteristics, with progression of tumour size and a higher risk of metastatic lymph nodes. The purpose of this study was to investigate delayed breast cancer diagnosis after repeated recall for the same mammographic abnormality at screening.


This was a retrospective study performed in two cohorts of women enrolled in a mammography screening programme in the Netherlands. All women aged 50−75 who underwent biennial screening mammography either between January 1, 1997 and December 31, 2006 (cohort 1) or between January 1, 2007 and December 31, 2016 (cohort 2) were included.


The cohorts showed no difference in proportions of women with delayed breast cancer diagnosis of at least 2 years (2.2% versus 2.8%, P = 0.29). Most delays were caused by incorrect BI-RADS classifications after recall (74.2%). An increase in mean tumour size was seen when comparing sizes at initial false-negative recall and at diagnosis of breast cancer (P < 0.001).


The proportion of women with a long delay in breast cancer confirmation following repeated recall at screening mammography has not decreased during 20 years of screening. These delays lead to larger tumour size at detection and may negatively influence prognosis.

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Fig. 1: Patient example, repeated recall after previous false-negative recall.


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Author information




J.R.C.L.: Performed data collection, data analyses, and wrote the manuscript. A.C.V.: Helped perform data analyses and edit the manuscript. R.M.P.: Helped write and edit the manuscript. W.S.-P.: Helped write and edit the manuscript. M.J.B.: Helped write and edit the manuscript and helped perform data analyses. V.C.G.T.-H.: Helped write and edit the manuscript. L.E.M.D: Designed the study, helped in writing the manuscript and also edited the manuscript. Also maintains database on screening outcome in the South of the Netherlands.

Corresponding author

Correspondence to Joost R. C. Lameijer.

Ethics declarations

Ethics approval and consent to participate

The Dutch Central Committee on Research Involving Human Subjects the Netherlands (CCMO) is the National Competent Authority supervising the ethical review of trials performed within the Netherlands. They have confirmed that approval for this study was not necessary. The descriptive study has been set up complementary to a screening program for which the Dutch Health Care Minister has provided a permit. As the subjects included in the complementary trial did not undergo any additional burden, the Dutch Research Involving Human Subjects Act does not warrant ethical approval for the trial. This study was performed in accordance with the Declaration of Helsinki. All women except one (who was excluded) gave consent to participate in this study.

Data availability

Data are stored in a database maintained by one of the authors (L.E.M.D). The data are not publicly available. When data are needed, an official request can be made through the Department of Radiology of the Canisius Wilhelmina Hospital Nijmegen.

Competing interests

The authors declare no competing interests.

Funding information

This research is funded by The Dutch Health Care Insurance Board, which also finances and provides national coordination for the breast cancer screening program.

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Lameijer, J.R.C., Voogd, A.C., Pijnappel, R.M. et al. Delayed breast cancer diagnosis after repeated recall at biennial screening mammography: an observational follow-up study from the Netherlands. Br J Cancer 123, 325–332 (2020). https://doi.org/10.1038/s41416-020-0870-2

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