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BREAST
Breast cancer screening in women with extremely dense breasts
recommendations of the European Society of Breast
Imaging (EUSOBI)
Ritse M. Mann
1,2
&Alexandra Athanasiou
3
&Pascal A. T. Baltzer
4
&Julia Camps-Herrero
5
&Paola Clauser
4
&
Eva M. Fallenberg
6
&Gabor Forrai
7
&Michael H. Fuchsjäger
8
&Thomas H. Helbich
4
&Fleur Killburn-Toppin
9
&
Mihai Lesaru
10
&Pietro Panizza
11
&Federica Pediconi
12
&Ruud M. Pijnappel
13,14
&Katja Pinker
4,15
&
Francesco Sardanelli
16,17
&Tamar Sella
18
&Isabelle Thomassin-Naggara
19
&Sophia Zackrisson
20
&
Fiona J. Gilbert
9
&Christiane K. Kuhl
21
&On behalf of the European Society of Breast Imaging (EUSOBI)
Received: 28 July 2021 / Revised: 21 January 2022 / Accepted: 27 January 2022
#The Author(s) 2022
Abstract
Breast density is an independent risk factor for the development of breast cancer and also decreases the sensitivity of mammog-
raphy for screening. Consequently, women with extremely dense breasts face an increased risk of late diagnosis of breast cancer.
These women are, therefore, underserved with current mammographic screening programs. The results of recent studies reporting
on contrast-enhanced breast MRI as a screening method in women with extremely dense breasts provide compelling evidence
that this approach can enable an important reduction in breast cancer mortality for these women and is cost-effective. Because
there is now a valid option to improve breast cancer screening, the European Society of Breast Imaging (EUSOBI) recommends
that women should be informed about their breast density. EUSOBI thus calls on all providers of mammography screening to
share density information with the women being screened. In light of the available evidence, in women aged 50 to 70 years with
extremely dense breasts, the EUSOBI now recommends offering screening breast MRI every 2 to 4 years. The EUSOBI
acknowledges that it maycurrently not bepossible to offer breast MRI immediately and everywhere and underscores that quality
assurance procedures need to be established, but urges radiological societies and policymakers to act on this now. Since the
wishes and values of individual women differ, in screening the principles of shared decision-making should be embraced. In
particular, women should be counselled on the benefits and risks of mammography and MRI-based screening, so that they are
capable of making an informed choice about their preferred screening method.
Key Points
•The recommendations in Figure 1 summarize the key points of the manuscript
Keywords Early detection of cancer .Breast density .Mammography .Magnetic resonance imaging .Decision-making, shared
Abbreviations
ACR American College of Radiology
BI-RADS Breast Imaging –Reporting and Data System
DBT Digital breast tomosynthesis
DM Digital mammography
EUSOBI European Society of Breast Imaging
FFDM Full-field digital mammography
MRI (Breast) Magnetic resonance imaging
PPV Positive predictive value
QALY Quality-adjusted life year
WHO World Health Organisation
Introduction
Breast density describes the amount of fibroglandular tissue in
the breast relative to the amount of fatty tissue. The epithelial
structures within the breast, i.e. the glandular lobes and the
ducts, are part of this fibroglandular tissue; therefore, breast
*Ritse M. Mann
ritse.mann@radboudumc.nl; r.mann@nki.nl
Extended author information available on the last page of the article
European Radiology
https://doi.org/10.1007/s00330-022-08617-6
cancer mostly originates from this tissue. The amount of
fibroglandular tissue is largely genetically determined and de-
pends on hormonal stimulation. It usually decreases over time,
particularly after menopause.
The fibroglandular tissue absorbs ionizing radiation (x-
rays) and projects white on mammography. Consequently, it
is commonly referred to as ‘dense’tissue. Since most cancers
absorb x-rays to a similar extent as fibroglandular tissue, can-
cers manifest as white masses on mammograms. Dense
(white) tissue on mammograms can therefore hide the similar-
ly dense (white) cancers. This means that dense tissue may
prevent the detection; i.e., it can ‘mask’cancers on mammog-
raphy [1]. Only the small fraction of cancers that contain cal-
cifications is reasonably well seen on mammography indepen-
dent of the amount of dense tissue.
The distribution of the individual amount of fibroglandular
tissue, and thus of mammographic densities across the female
population, follows a typical bell-shaped curve (Gaussian dis-
tribution) of many biological features. In clinical practice, this
biologic continuum is categorized in four large bins and is
described according to the ACR BI-RADS atlas terminology
as follows [2]:
a. The breasts are almost entirely fatty (about 10% of the
screening population [3])
b. There are scattered areas of fibroglandular density (about
42% of the screening population)
c. The breasts are heterogeneously dense, which may ob-
scure small masses (about 40% of the screening
population)
d. The breasts are extremely dense, which lowers the sensi-
tivity of mammography (about 8% of the screening
population)
The latter two categories are commonly referred to as
‘dense’breasts.
Although visual assessment of density is known to have a
relatively high intra- and inter-reader variability, the visual
estimation of density has been reported to have a somewhat
higher correlation with breast cancer risk than automated as-
sessments [4–6]. However, to minimize variability in the se-
lection of women for supplemental or alternate screening
based on breast density,automated methods may bepreferable
[4–6].
Besides the risk of masking breast cancer, women with
extremely dense breasts in the screening age range have an
increased risk of developing breast cancer, which is approxi-
mately twice as high as for the ‘average’woman, and almost
4–6 times as high as in women with almost entirely fatty
breasts [1,7]. This is due to both the absolute higher amount
of fibroglandular tissue within the breast and the breast com-
position [8]. Breast density is independent of other personal
risk factors typically used for breast cancer risk prediction, and
complementary when used in conjunction [9,10]. Breast den-
sity is estimated to account for 26% of breast cancers in post-
menopausal women [11]. Moreover, a higher breast density
has also been associated with an increased breast cancer-
specific mortality [12], albeit this data is not consistent among
studies [13,14].
Current evidence on breast cancer screening
in women with dense breasts
Screening is widely regarded as one of the most successful
approaches to reducing breast cancer mortality in average-risk
women and is recommended by the WHO [15] as well as
EUSOBI [16]. Based on a meta-analysis of randomized con-
trolled trials reporting on population screening, offering mam-
mography screening to women aged 50–70 reduces breast
cancer mortality by 20% [17]. Case-control studies in women
actually screened show an even substantially higher mortality
reduction of approximately 40% [18].
And yet, unfortunately, current screening strategies still
fail to prevent death due to breast cancer in a substantial
proportion of women: Among every 1000 women
screened, in 8 disease-specific death is averted, but 11 still
die from breast cancer [19]. This is due to the failure of
timely detection of biologically relevant breast cancers, i.e.
underdiagnosis.
Underdiagnosis is more of a problem in women with extreme-
ly dense breast tissue compared to other women. In women with
largely fatty breasts, the sensitivity of mammography screening
is 86 to 89%, meaning that only 11 to 14% of cancers present as
interval cancer in between two screening rounds. This program
sensitivity decreases to 62–68% in women with extremely dense
breasts [20]. For full-field digital mammography (FFDM) similar
poor figures were reported, with a program sensitivity of only
61% based on biannual screening [21]. There is currently little
data on interval cancers by density for digital breast
tomosynthesis (DBT), but it is unlikely that tomosynthesis is
going to overcome the reduction in sensitivity caused by density.
Several studies reported increased cancer detection rates by 20 to
40% also in women with (extremely) dense breasts [22,23],
mainly due to the detection of more spiculated masses and archi-
tectural distortions, but there is only limited evidence that this
leads to reduced rates of interval cancers in these women.
According to Conant et al, the sensitivity of DM and DBT was
similarly based upon 1-year follow-up [23]. X-ray-based ana-
tomic imaging modalities—being either screen-film mammogra-
phy, FFDM or DBT—all seem to be heavily affected by breast
density and thus lead to underdiagnosis of relevant cancers in
these women.
Several studies have investigated supplemental ultrasound
as a technique to improve the performance of population-
based screening in women with extremely dense breasts
Eur Radiol
[24–28]. On average, cancer detection increases by 2.3/1000
screens with ultrasound [26]. The added detection with ultra-
sound is also present when DBT screening is performed [27]
and persists in follow-up rounds [26,28]. Unfortunately, the
number of false-positive examinations strongly increases with
ultrasound. Reported positive predictive values for biopsy
vary widely, but are commonly below 10% for findings only
observed at ultrasound [26] and remain relatively low,even as
specificity increases in follow-up rounds [28]. In a large pro-
spective Japanese study conducted in women aged 40–49
years, it was shown that program sensitivity improved from
77 to 91% with the addition of an ultrasound examination
[25]. Moreover, they showed that the frequency of interval
cancer was reduced by 50%. Nevertheless, it is not clear
whether these findings can be considered a valid reference
for European screening programs, where screening focuses
on women aged 50–69, where the incidence of breast cancer
is much higher and where women tend to have larger, more
heterogeneous breasts; the results do provide initial evidence
to suggest that, for some women, ultrasound may be beneficial
[24–29]. Within Europe, supplemental ultrasound has been
structurally implemented in Austria for women with dense
breasts (BI-RADS classes c and d). In the timeframe from
2014 to 2017, the program showed a sensitivity of 71% and
a specificity of 99%. The breast cancer detection rate was
similar to EU standards. However, currently, the added value
of supplemental ultrasound regarding cancer detection is lim-
ited [30].
Accordingly, so far, these results have been insufficient for
EUSOBI to recommend that average-risk women undergoing
mammographic screening should be informed about their
breast density [16].
This reluctance was explained by the following facts:
&We were not convinced that the benefit/risk ratio of sup-
plemental screening for women with extremely dense
breasts was positive.
&Many European countries do not offer any form of sup-
plemental screening.
&Informing women about their density, in absence of high-
level scientific evidence for screening alternatives, could
increase anxiety and reduce screening participation.
However, this policy is now to change.
This change is prompted by an analysis of results of recent
screening studies with contrast-enhanced breast MRI, partic-
ularly the DENSE trial and the EA1411 ECOG-ACRIN study.
The DENSE trial is a Dutch nationwide multicenter ran-
domized trial in women with extremely dense breast tissue—
as automatically assessed by a computer program (Volpara)—
with a normal mammographic screening result [31].
Of the women invited for contrast-enhanced MRI, 59%
agreed to participate (4783/8061) and underwent MRI
screening. Supplemental MRI detected an additional 16.5 can-
cers /1,000 screens in the first round.
The interval cancer rate was 0.8/1,000, compared to 4.9/
1,000 in women invited but not participating and 5.0/1,000 in
women in the control group (n= 32,312). In other words,
undergoing supplemental MRI screening reduces the frequen-
cy of interval cancers by 84%, thus effectively reducing un-
derdiagnosis. The number of benign findings leading to recall
was 79.8/1,000 with MRI screening. The PPV of MRI
prompted biopsy was 26.3%, which we deem acceptable be-
cause it is similar to the PPV of biopsy reported for
mammography.
That MRI indeed detects breast cancers earlier is also ap-
parent from the number of cancers detected at the subsequent
mammographic screening round, which was 2.0/1,000, as
compared to 6.8/1,000 in the regular population of women
with extremely dense breasts.
Furthermore, the next MRI screen (2 years later) yielded a
supplemental detection rate of only 5.9/1,000, all of which were
stage 0/1 and node-negative; providing further evidence that
relevant cancers are detected predominantly earlier. Moreover,
the number of benign lesions leading to recall becomes much
smaller in the follow-up round (28.4/ 1,000), and therefore, the
PPV remained stable (PPV = 23.5% in follow-up) [32].
The results of the DENSE trial have been modelled in a
microsimulation model (MISCAN) to determine the long-
term impact of offering breast MRI screening to women with
extremely dense breasts [33]. This model was also used to
explore other scenarios, for which the model used the mea-
sured sensitivity and specificity of mammography and MRI as
observed in the DENSE trial, plus the estimated biological
behavior of breast cancers, and information on the efficacy
of treatment of breast cancers obtained from historical data.
The results of this microsimulation model suggest that adding
biennial MRI to biennial mammography—as was performed
in the DENSE trial—would save 8.6 additional lives per 1,000
women invited, at a cost of 150,000 Euro per life, or 22,500
Euro per quality-adjusted life-year (QALY). While this is al-
ready deemed cost-effective, alternative strategies using MRI
alone (without mammography) dominate this strategy in the
model. For example, using MRI alone once every 4 years
could be regarded as the most cost-effective screening strate-
gy. This would save 7.6 additional lives per 1,000 women
screened at a cost of 75,000 Euro per life or 11,500 Euro per
QALY. In practice, MRI alone with a frequency of onceevery
2 to 3 years may be preferred to prevent non-detection of
rapidly growing cancers, although a higher frequency may
also lead to a somewhat higher false positive rate (see below).
As the costs ofMRI screening are mostly influenced by the
cost of the MR scans [33], there is strong interest in breast
MRI with shorter scan protocols, generally referred to as ab-
breviated breast MRI. This may enable a higher throughput
and therefore a lower cost per examination.
Eur Radiol
The EA1411 ECOG-ACRIN study was an international
study (mainly conducted in the USA) with 48 sites in academ-
ic, community hospital, and private practice settings. It includ-
ed 1,444 women with dense breasts (heterogeneously dense—
category c, or extremely dense—category d), who underwent
routine screening both by DBT and abbreviated MRI. Both
screening methods were conducted in randomized order and
read strictly independently of each other, in order not only to
compare the performance of abbreviated MRI with that of
DBT, but to also investigate the use of abbreviated MRI as a
stand-alone screening method [34]. MRI protocols were var-
iable, but were all shorter than 10 min. In the first screening
round of the EA1141 study, overall cancer detection rate with
MRI was 15.2/1,000, as compared to 6.2/1,000 for DBT.
Respective sensitivity was 95.7% versus 39.1%. No interval
cancers were observed. The positive predictive value for bi-
opsy was somewhat lower for MRI (19.6% versus 31%), al-
though not statistically significantly different. This is likely
caused by the fact that a prior DBT needed to be available
(i.e. this was a follow-up DBT screening examination), where-
as none of the participants could have had a prior MRI (i.e.
this was a first-round MRI examination). In summary, the
ECOG-ACRIN EA1141 study shows that abbreviated MRI
can have a similar success as the standard MRI protocol that
was used within the DENSE trial. Moreover, the study pro-
vided further evidence that in women undergoing MRI for
screening, the additional contribution of x-ray-based breast
imaging is very limited [34].
In summary, there is cumulating evidence on the fact that
women with dense breasts are underserved by screening with
mammography or DBT alone. This evidence is available for
both women with heterogeneously dense as well as extremely
dense breasts. For the latter, there is now level I evidence
available on the efficacy of MRI screening on reducing un-
derdiagnosis and breast cancer-specific mortality, and on an
improved benefit-risk balance of screening compared to reg-
ular, mammographic screening. While for women with het-
erogeneously dense breasts MRI may also improve cancer
detection, the risk-benefit balance is currently less clear.
Consequently, EUSOBI will now recommend MRI screen-
ing in women with extremely dense breasts as specified in the
“EUSOBI recommendations on screening women with dense
breasts”section. This recommendation is independent of other
recommendations for screening in women at increased risk
due to, for example, family history or a personal history of
breast cancer. The evidence is strongest for women aged 50 to
70. However, it could be considered to adopt the recommen-
dations from the age at which screening is started when this is
different.
Despite the currently available evidence, it is likely not
possible to implement MRI screening for women with ex-
tremely dense breasts immediately and everywhere.
Differences in the availability of equipment, staff and
experience and the general willingness of policymakers to
pay for screening tests vary from country to country and will
affect the level to which these recommendations can and will
be implemented.
When implementing MRI screening, it is essential to stan-
dardize the examinations, educate technologists, radiologists
and other involved professionals, and monitor the quality of
images acquired. Radiologists’performance must also be
monitored with a specific focus on the prevention of false-
positive recalls, as these are considered a major burden to
the healthy female population. The availability of MR-
guided biopsy is essential for the introduction of breast MRI
as a screening technique [35].
Recommendations on how to inform women
Physicians who counsel women about their respective choices
regarding breast cancer screening in general, and screening in
women with extremely dense breasts in particular, must have
expertise in the principles of screening in general, and in
screening by imaging in particular.
Such expertise is usually not routinely available in primary
healthcare providers.
Accordingly, EUSOBI urges radiologists to assume this
important task and directly engage in informing women about
the pros and cons of screening. Educating other healthcare
providers might be another way to ensure that women receive
correct and objective information. The following passages
may serve as a guide for women’seducation;
How to explain the advantages associated with breast
MRI screening in women with extremely dense
breasts
Based on the modelled results of the DENSE trial [31,33], it is
through the following:
&A woman with extremely dense breasts who is never
screened has a chance of a little over 5 % to die from breast
cancer.
&Participation in screening with mammography every other
year leads to early detection of cancer in about 7 % of
women and reduces the likelihood to die of breast cancer
to just over 4 %, i.e. reduces the risk to die of breast cancer
by 20%.
&According to epidemiological modelling of DENSE trial
results, participation in screening with MRI every other
year leads to early cancer detection in about 10% of wom-
en and reduces the risk to die from breast cancer to a little
over 3%, providing a mortality reduction by about 40 %.
&According to epidemiological modelling of DENSE trial
results, when dying from breast cancer is prevented by
Eur Radiol
MRI, a woman gains on average 15 years in good health,
before she dies of another cause.
&For women who would have survived breast cancer also in
absence of screening, the benefit is mainly that earlier
detection of breast cancer might enable less aggressive
treatment.
This reduced mortality, and potentially less aggressive
treatment, comes at a price.
How to explain the disadvantages associated with
breast MRI screening:
In essence, screening in general, as well as screening by MRI
in particular, has three relevant disadvantages. Women should
also be thoroughly informed about these downsides of screen-
ing in order to be able to make informed choices.
First, the need to undergo the screening test
For women with extremely dense breasts, this currently im-
plies undergoing a mammogram at least once, i.e. at the start
of screening, to establish the presence of extremely dense
breasts, and then contrast-enhanced breast MRI, either as a
supplemental or stand-alone screening test, once every 2 to 4
years.
Hence, she should be informed about the need for an IV
cannulation, the administration of an intravenous contrast
agent and the nature of a 10-min MRI examination [35,36].
While these examinations are in general well accepted, they
are not perceived as pleasant. The administration of contrast
agent implies that there is a very small risk for non-negligible
(allergic) contrast reactions. Notably, these allergic or pseudo-
allergic reactions arerare, and the vast majorityof these events
are mild.
Possible side effects of the contrast agent are as follows
[37]:
&Occasionally (about 1 in 100): headache or nausea.
&Rare (less than 1 in 1,000): anaphylactoid or mild anaphy-
lactic reactions leading to rash, mild drop in blood pres-
sure, tachycardia, not requiring specific treatment.
&Extremely rare (less than 1 in 1,000,000): severe hyper-
sensitive reactions (anaphylactoid or anaphylactic) with
cardiovascular, respiratory of cutaneous manifestations,
ranging from mild to severe, potentially life-threatening.
Second, the possibility of false-positive screening findings
Whenever screening findings are abnormal, further assess-
ment is required to establish a final diagnosis to finally decide
whether the finding represents breast cancer or not. Where this
assessment confirms the presence of breast cancer, the respec-
tive screening finding is considered ‘true-positive’;whenthe
assessment proves the presence of a benign change, but no
breast cancer, the respective screening finding is considered
‘false positive’—possibly better understood when referred to
as ‘false alarm’.
Women should be informed that supplemental screening
tests in general, and screening with breast MRI in particular,
when used over several years or even decades, will increase
the chance that she will at least once experience the situation
of a ‘false alarm’, i.e. receive a positive screening test which,
after appropriate assessment, turns out to be a harmless find-
ing. Of all positive (abnormal) screening findings, only about
30% are really cancerous; this value is similar for mammog-
raphy and for MRI.
Women should also be informed about the fact that the
‘assessment’to find out whether a positive screening finding
corresponds to cancer or not will consist of some additional
imaging studies for most, and/or of minimally-invasive needle
biopsy for some women. Particularly the latter is an unpleas-
ant and somewhat painful, yet generally well accepted, proce-
dure [38]. Regardless, it is essential to minimize the need for
additional procedures. Based on current literature, with mam-
mographic screening approximately 1 in 7 women will ever
need additional imaging or biopsy, with 2 or 4 yearly MRIs;
this number may increase toapproximately 1 in 4 to 5 women.
Where the assessment confirms the absence of breast can-
cer, in other words: In women where the screening finding
was false-positive, women may have experienced (eventually
unnecessary) fear of having breast cancer for a few days until
the assessment results are available. Therefore, effort should
be made to avoid false-positive findings altogether and to keep
the time to the final diagnosis short.
No woman should ever be treated for breast cancer because
of a false-positive screening finding. Only when pathologic
review undoubtedly shows cancerous tissue should women
receive treatment for breast cancer.
Third, the possibility of overdiagnosis
A number of cancers detected during screening would never
have become symptomatic before the affected woman would
have died of other causes. Diagnosis of such cancers is re-
ferred to as ‘overdiagnosis’. Unfortunately, overdiagnosis is
not knowable at the individual level at the time of cancer
detection. In practice, these women will generally be treated
for their disease as currently there is no reliable method to
determine whether a specific cancer is life-threatening or rep-
resents an ‘overdiagnosis’.
Based on the modelled DENSE data, about 25% of
mammographically detected cancers (in 1.7% of women)
and about 22% of MRI detected cancers (in 2.1% of women)
may represent overdiagnosis [33]. These are mainly the low
Eur Radiol
grade in situ, and some very indolent invasive breast cancers.
Treatment is tailored to the specific biology of the disease in a
given patient. Hence, while overdiagnosis cannot be
prevented; the effect is mitigated by adapting the treatment
to the aggressiveness of the detected cancer.
Shared decision-making
Screening in general, and MRI screening in particular may be
lifesaving. However, it should be realized that, although breast
cancer is by far the most frequent type of cancer in women,
and although it still represents the most or second-to-most
important cause of cancer death in women, the vast majority
of women (> 85%) will never develop breast cancer during
their lifetimes.
Thus, while all women should be invited to undergo breast
cancer screening, only a minority will ever be diagnosed with
breast cancer, and only those women can benefit from early
diagnosis. The remaining women will never develop breast
cancer and in these women, undergoing screening cannot be
beneficial (other than assuring a woman that she does not have
breast cancer), but can only have negative side effects. From a
populationstandpoint, the (substantial) benefit for the relative-
ly few women who do develop breast cancer justifies the side
effects of screening for the vast majority who remain cancer-
free.
Still, mammographic screening is commonly criticized be-
cause of false-positive findings and overdiagnosis. Even
though the benefit/risk ratio increases with MRI screening,
in absolute numbers, both the number of false-positive screen-
ing tests and the number of overdiagnoses increase. For the
individual woman, the recognized side effects may be argu-
ments to deviate from the population-based screening advice.
This must be respected.
Choosing not to attend a given screening program, or
opting for a less efficient screening method, should be a
choice that resides with the individual woman herself.
Such a choice is a personal decision that should never be
criticized, nor penalized, not even indirectly. However, to
enable women to make an informed decision, they must be
well informed by their radiologists (breast imagers) and
should be able to place this information in the context of
their preferences and values.
This is the hallmark of shared decision-making. In partic-
ular for screening, where multiple options are viable and jus-
tifiable, this participatory process is absolutely essential.
It obviously also implies that there is an obligation for the
medical community to offer techniques that are proven
effective; otherwise, the freedom of choice is essentially
denied.
It should be noted that true application of shared decision-
making clashes with current measures of the effectiveness of
screening programs that assess quality—among other
things—mainly by considering the overall participation rate.
Although this is sound from a public healthcare perspective, it
ignores the fact that individual women’s needs, priorities and
values differ. What appears perfectly acceptable to one wom-
an may be unacceptable to another. Of course, achieving or
demonstrating a reduction of mortality on a population-wide
level requires high participation rates. However, these con-
cerns should not preclude or delay the recommendation of
imaging tests that can effectively avoid premature death from
breast cancer in individual women, even if such tests are not
yet widely available.
Consequently, we should move away from evaluating the
participation rate of a one-size-fits-all screening program to-
wards more personalized screening. We should start assessing
how a multifaceted screening program fits with the wishes of
the women we intend to serve.
Further considerations
This recommendation is only applicable to women with
extremely dense breasts. Although women with less dense
breasts, e.g. those with heterogeneously dense breasts,
might also benefit from other screening approaches, the
evidence in this field is currently insufficient to make
strong recommendations for practice. Rather, we urge
the medical community to also investigate the value of
MRI screening for women with less dense breast tissue
in high-quality trials.
In the future, other factors than breast density alone
couldbeusedtoselectwomenataverageriskwhowould
benefit most from MRI screening. For example, density
could be combined with classic risk calculators in order to
select a smaller fraction of women at higher risk for MRI
screening [9,39]. Likewise, patient selection using AI-
assessment of screening mammograms could be employed
as this would likely allow earlier detection of cancers in
women with less dense breasts too [40]. However, these
approaches are currently not validated in prospective stud-
ies, and it remains therefore uncertain whether they could
achieve similar or even better results than the selection of
women based upon density alone. Still, in the future, this
mayleadtootherselectioncriteriaforMRIscreening
than we currently recommend.
Eur Radiol
Fig. 1 EUSOBI summary recommendations on screening women with extremely dense breasts
Eur Radiol
Due to continuous technical innovation, other imaging mo-
dalities may eventually offer practical advantages over the
currently proposed contrast-enhanced breast MRI examina-
tions, including contrast-enhanced mammography, several
ultrasound-based techniques, MRI sequences without intrave-
nous contrast administration and isotope-based imaging tests
[41]. Unfortunately, most of these techniques have not (or
only marginally) been tested in screening and any assumption
about their efficacy is therefore premature. Still, some of these
techniques could be considered in women at increased breast
cancer risk with contraindications to MRI screening as they
have a proven higher clinical sensitivity than mammography.
EUSOBI recommendations on screening
women with dense breasts
In women with extremely dense breast tissue at average
risk, underdiagnosis of relevant breast cancers is a ma-
jor challenge, even with high-quality 2D digital mam-
mography or DBT screening. Therefore, these women
are underserved by current mammographic screening
programs.
In view of all the above, the EUSOBI has decided to adopt
the recommendation for breast cancer screening provided in
Fig. 1
Acknowledgements The authors wish to thank Dr. EAM Heijnsdijk for
providing supplemental insight into the cost-effectiveness analysis of the
DENSE trial.
Funding The authors state that this work has not received any funding.
Declarations
Guarantor The scientific guarantor of this publication is R. M. Mann.
Conflict of interest All authors are members of the current executive
board of the European Society of Breast Imaging (EUSOBI). The docu-
ment reflects the current position of EUSOBI. The authors report no
relevant disclosures to the contents of this work.
Statistics and biometry No complex statistical methods were necessary
for this paper.
Informed consent Not applicable
Ethical approval Institutional Review Board approval was not required
because this is a society recommendation.
Methodology
•Expert consensus based on the current literature assessment
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Publisher’snote Springer Nature remains neutral with regard to jurisdic-
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Eur Radiol
Affiliations
Ritse M. Mann
1,2
&Alexandra Athanasiou
3
&Pascal A. T. Baltzer
4
&Julia Camps-Herrero
5
&Paola Clauser
4
&
Eva M. Fallenberg
6
&Gabor Forrai
7
&Michael H. Fuchsjäger
8
&Thomas H. Helbich
4
&Fleur Killburn-Toppin
9
&
Mihai Lesaru
10
&Pietro Panizza
11
&Federica Pediconi
12
&Ruud M. Pijnappel
13,14
&Katja Pinker
4,15
&
Francesco Sardanelli
16,17
&Tamar Sella
18
&Isabelle Thomassin-Naggara
19
&Sophia Zackrisson
20
&
Fiona J. Gilbert
9
&Christiane K. Kuhl
21
&On behalf of the European Society of Breast Imaging (EUSOBI)
1
Radboud University Medical Center, Geert Grooteplein Zuid 10,
6525 GA Nijmegen, Netherlands
2
The Netherlands Cancer Institute, Plesmanlaan 121, 1066
CX Amsterdam, Netherlands
3
Breast Imaging Department, MITERA Hospital, 6, Erithrou Stavrou
Str. 151 23 Marousi, Athens, Greece
4
Department of Biomedical Imaging and Image-guided Therapy,
Division of General and Pediatric Radiology, Research Group:
Molecular and Gender Imaging, Medical University of Vienna,
Währinger Gürtel 18-20, 1090 Wien, Austria
5
Hospitales Ribera Salud, Avda.Cortes Valencianas, 58,
46015 Valencia, Spain
6
Department of Diagnostic and Interventional Radiology, School of
Medicine &; Klinikum Rechts der Isar, Technical University of
Munich, Munich (TUM), Ismaninger Str. 22,
81675 München, Germany
7
Departmentof Radiology, Duna Medical Center, Budapest, Hungary
8
Division of General Radiology, Department of Radiology, Medical
University Graz, Auenbruggerplatz 9, 8036, Graz, Austria
9
Department of Radiology, University of Cambridge, Cambridge
Biomedical Campus, Hills road, Cambridge CB20QQ, UK
10
Radiology and Imaging Laboratory, Carol Davila University,
Bucharest, Romania
11
Breast Imaging Unit, IRCCS Ospedale San Raffaele,, Via Olgettina
60, 20132 Milan, Italy
12
Department of Radiological, Oncological and Pathological
Sciences, Sapienza University of Rome, Viale Regina Elena, 324,
00161 Rome, Italy
13
Department of Imaging, University Medical Centre Utrecht, Utrecht
University, Heidelberglaan 100, 3584 CX Utrecht, Netherlands
14
Dutch Expert Centre for Screening (LRCB), Wijchenseweg 101,
6538 SW Nijmegen, Netherlands
15
Department of Radiology, Breast Imaging Service, Memorial Sloan
Kettering Cancer Center, 300 E 66th Street, New York, NY 10065,
USA
16
Unit of Radiology, IRCCS Policlinico San Donato, San Donato
Milanese, Milan, Italy
17
Department of Biomedical Sciences for Health, Università degli
Studi di Milano, Via Morandi 30, 20097 San Donato Milanese,
Milan, Italy
18
Department of Diagnostic Imaging, Hadassah Hebrew University
Medical Center, Jerusalem, Israel
19
Department of Radiology, Sorbonne Université, APHP, Hôpital
Tenon, 4, rue de la Chine, 75020 Paris, France
20
Diagnostic Radiology, Department of Translational Medicine,
Faculty of Medicine, Lund University, Skåne University Hospital
Malmö, SE-205 02 Malmö, Sweden
21
University Hospital of Aachen, Rheinisch-Westfälische Technische
Hochschule, Pauwelsstraße30, 52074 Aachen, Germany
Eur Radiol
