Letter to the Editor
Mammography Screening and Breast Cancer Mortality—Response
Suzie J. Otto
1
, Jacques Fracheboud
1
, Andr e L.M. Verbeek
2
, Rob Boer
1
,
Jacqueline C.I.Y. Reijerink-Verheij
3
, Johannes D.M. Otten
2
, Mireille J.M. Broeders
2,4
, and
Harry J. de Koning
1
, for the National Evaluation Team for Breast Cancer Screening
We thank Drs. Autier and Boniol for their comment
raised on the outcome of our case–control study on the
impact of mammography screening on the risk of
death from breast cancer, but we feel that the metho-
dologic limitations inherent to the case–control design
are small.
Aarts and colleagues (1) indeed showed that the par-
ticipation rate among women of high socioeconomic sta-
tus (SES) is somewhat higher than those of low SES (87%
vs. 79%), in the Netherlands mostly coinciding with
women of non-Western ethnic descent. The attendance
rate is lower in this group of women (2), in which breast
cancer incidence is also considerably lower (3) as well as
the risk of death from breast cancer than in the native
Dutch population (4).
Aarts and colleagues further report that low SES
women are diagnosed with prognostically less favorable
breast cancers. However, these differences in tumor
stage and overall survival were observed among nonpar-
ticipants as well as participants, either screen-detected or
symptomatically diagnosed interval breast cancer (1).
Therefore, it is incorrect to deduce that participants and
nonparticipants present with genuine differences in risk
factors associated with dying from breast cancer or
from other causes. Risk differences associated with SES
groups would reflect only very partially in risk differ-
ences between participants and nonparticipants. Case–
control studies that could adjust for SES showed no effect
of this correction on the estimated ORs (5).
Autier and Boniol question the validity of the factor
used for correction of self-selection bias, which is calcu-
lated as the relative risk (RR) of death from breast cancer
among nonparticipants compared with uninvited wom-
en. We used individual data on breast cancer mortality in
nonparticipants from the study period 1990 to 2003 and,
due to privacy regulations, aggregated data on uninvited
women from the prescreening period (1986–1989). Our RR
of 1.11 was remarkably similar to the RR of 1.08 from
another Dutch study (6) that used data on contempora-
neous groups of nonparticipants and uninvited women
in the implementation period for screening (1990–1995)
from the same region. If breast cancer mortality after 1990
has been decreasing among nonparticipants (numerator
of the RR) due to better treatment, then this would
also apply for not invited women (denominator of the
RR). The RR would then approach unity and results in a
higher effect of screening on the risk of breast cancer
mortality, adjusted for self-selection. There is no evidence
of differential treatment. As screening is fully implemen-
ted in the Netherlands, estimation of a correction factor for
more recent years is hampered, but given the stable
attendance rate in the Netherlands, there is little reason
to believe that this will change considerably. Thus, in
organized breast cancer screening programs, self-selec-
tion appears to be relatively minor.
In our case–control study, we minimized the biases
inherent to an observational study design (e.g., identifi-
cation and selection of cases and controls, equal access to
screening during the exposure period, definition of expo-
sure, source population). We showed that breast cancer
screening resulted in a 49% reduced risk of dying of breast
cancer for women invited and attended mammography
screening. Observational study designs are crucial for the
evaluation of the effect of mammography screening in the
actual female population.
Disclosure of Potential Conflicts of Interest
No potential conflicts of interests were disclosed.
Received February 22, 2012; accepted February 23, 2012; published
OnlineFirst March 8, 2012.
References
1. Aarts MJ, Voogd AC, Duijm LE, Coebergh JW, Louwman WJ. Socio-
economic inequalities in attending the mass screening for breast
cancer in the south of the Netherlands–associations with stage at
diagnosis and survival. Breast Cancer Res Treat 2011;128:517–25.
2. Vermeer B, van den Muijsenbergh METC. The attendance
of migrant women at the national breast cancer screening
in the Netherlands 1997–2008. Eur J Cancer Prev 2010;19:
195–8.
Authors' Affiliations:
1
Department of Public Health, Erasmus MC, Uni-
versity Medical Center Rotterdam;
2
Department of Epidemiology, Biosta-
tistics and HTA, Radboud University Nijmegen Medical Centre;
3
Cancer
Screening Organization for Southwest Netherlands, Rotterdam; and
4
National Expert and Training Centre for Breast Cancer Screening, Nijme-
gen, the Netherlands
Corresponding Author: Suzie J. Otto, Erasmus MC, University
Medical Center Rotterdam, P.O. Box 2040, Rotterdam 3000 CA,
the Netherlands. Phone: 31-10-7043446; Fax: 31-10-7038474;
E-mail: s.otto@erasmusmc.nl
doi: 10.1158/1055-9965.EPI-12-0235
Ó2012 American Association for Cancer Research.
Cancer
Epidemiology,
Biomarkers
& Prevention
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Published OnlineFirst March 8, 2012; DOI: 10.1158/1055-9965.EPI-12-0235