Eur Radiol (2010) 20: 1624

DOI 10.1007/s00330-009-1523-2 BREAST

Hendrik J. Teertstra
Claudette E. Loo
Maurice A. A. J. van den Bosch
Harm van Tinteren
Emiel J. T. Rutgers
Sara H. Muller
Kenneth G. A. Gilhuijs
Received: 5 November 2008
Revised: 3 June 2009
Accepted: 13 June 2009
Published online: 6 August 2009
# European Society of Radiology 2009
Breast tomosynthesis in clinical practice:
initial results
Abstract The purpose of this study
was to assess the potential value of
tomosynthesis in women with an
abnormal screening mammogram
or with clinical symptoms.
Mammography and tomosynthesis
investigations of 513 woman with
an abnormal screening mammogram
or with clinical symptoms were
prospectively classified according
to the ACR BI-RADS criteria. Sensi-
tivity and specificity of both tech-
niques for the detection of cancer were
calculated. In 112 newly detected
cancers, tomosynthesis and
mammography were each false-
negative in 8 cases (7%). In the false-
negative mammography cases, the
tumor was detected with ultrasound
(n=4), MRI (n=2), by recall after
breast tomosynthesis interpretation
(n=1), and after prophylactic
mastectomy (n=1). Combining the
results of mammography and tomo-
synthesis detected 109 cancers.
Therefore in three patients, both
mammography and tomosynthesis
missed the carcinoma. The sensitivity
of both techniques for the detection of
breast cancer was 92.9%, and the
specificity of mammography and
tomosynthesis was 86.1 and 84.4%,
respectively. Tomosynthesis can be
used as an additional technique to
mammography in patients referred
with an abnormal screening mammo-
gram or with clinical symptoms.
Additional lesions detected by tomo-
synthesis, however, are also likely to
be detected by other techniques used in
the clinical work-up of these patients.
Keywords Breast
.
Mammography
.
Tomosynthesis
.
Cancer
.
Detection
Introduction
In western countries, breast cancer is the most common type
of cancer in women. In the Netherlands, the disease is
currently diagnosed in over 12,000 women each year. The
chance of developing breast cancer during a womans
lifetime is 910%. The impact of invasive breast cancer
increases with the size and extent of invasion at first
diagnosis [1]. In large cancers, surgery and radiotherapy will
be more aggressive, neo-adjuvant therapy is more often
needed, and the prognosis is worse. Therefore, accurate
diagnosis is essential for optimal treatment and for the
assessment of prognosis. Mammography is currently the first
choice of imaging investigation in symptomatic women
despite its well-known limitations. The false-negative rate of
mammography ranges from 8 to 66% in symptomatic
women, depending on factors such as breast density and
tumor type [211]. This apparent lack of sensitivity is
considered to be caused by the misinterpretation of
architectural distortion, asymmetrical density, and fibro-
glandular tissue overlapping the cancer, thus obscuring the
margins of the cancer.
Considering these limitations, the threshold for perform-
ing additional investigations in symptomatic patients with a
negative mammogram should be low. These additional
investigations include additional mammographic views
(compression, magnification), ultrasound [810], needle
sampling, and magnetic resonance imaging (MRI) for
H. J. Teertstra (*)
.
C. E. Loo
.
M. A. A. J. van den Bosch
.
S. H. Muller
.
K. G. A. Gilhuijs
Division of Radiology, The
Netherlands Cancer Institute-Antoni
van Leeuwenhoek Hospital,
Amsterdam, The Netherlands
e-mail: h.teertstra@nki.nl
Tel.: +31-20-5121094
H. van Tinteren
Division of Biostatistics, The
Netherlands Cancer Institute-Antoni
van Leeuwenhoek Hospital,
Amsterdam, The Netherlands
E. J. T. Rutgers
Division of Surgery, The Netherlands
Cancer Institute-Antoni van
Leeuwenhoek Hospital,
Amsterdam, The Netherlands
selected indications [1214]. The latter technique is
relatively expensive but has a high sensitivity (95100%)
for the detection of invasive cancer.
In recent years, new techniques have been introduced
aiming to improve the sensitivity of mammography for the
detection of breast carcinoma, including digital mammog-
raphy [1518], computer-aided diagnosis [1921], and
more recently breast tomosynthesis [15, 16, 1924].
Tomosynthesis of the breast is a three-dimensional radio-
graphic technique that obtains three-dimensional informa-
tion from 10 to 25 projection images, thereby reducing the
effects of structure overlap. In recent studies [16, 2324],
breast tomosynthesis was subjectively better than conven-
tional digital mammography in highlighting masses and
areas of architectural distortion.
Conversely, it was shown that calcifications were better
demonstrated with conventional mammography [16].
Tomosynthesis may also have the potential to decrease
the recall rate when used together with digital screening
mammography [21]. But despite the publication of these
studies, little is known on how to use tomosynthesis in
daily clinical practice and guidelines are lacking. This
study was designed to assess the potential additional value
of breast tomosynthesis compared to digital mammography
in women referred with an abnormal screening mammo-
gram or with clinical symptoms.
Materials and methods
The study was approved by the ethics committee of our
institute, and written informed consent was obtained from
all participating women.
Subjects
Women referred with an abnormal screening mammogram
(Dutch National Screening Program), with clinical symp-
toms, or referred from other hospitals for a second opinion
were seen by a breast surgeon or dedicated nurse practi-
tioner in our outpatient breast clinic. After clinical
examination these women were sent to the Radiology
Department. They underwent mammography and were
asked to participate in the study. After mammography,
further work-up was done when indicated, using ultrasound
and fine-needle aspiration biopsy (FNAB), if necessary
followed by core biopsy.
Digital mammography
Standard (two projections, CC and MLO) conventional
digital mammography (Lorad Selenia; Hologic, Bedford,
MA) was performed by technologists trained and experi-
enced in breast radiology.
Tomosynthesis
Subsequently, breast tomosynthesis was performed by
one of two dedicated technologists trained by Hologic
using a prototype manufactured by Hologic with a high-
resolution detector that has a surface area of 24
29 cm, comparable to standard digital mammography.
The breast tomosynthesis acquisition was as follows:
11 projection images were acquired in increments of
approximately 1.5 starting at 7.5 and ending at +7.5,
with the breast in standard compression, in both CC and
MLO projections. The total radiation exposure to the
patient during breast tomosynthesis acquisition was
adjusted so that it was comparable to that during
conventional digital mammography. Following the acqui-
sition, the 11 projection images were reconstructed into a
3D dataset [19].
Radiation dose
The mean glandular dose was estimated according to the
ACR technical standard [25], using as a phantom the
ACR Nuclear Associates model 18220, consisting of
4.5-cm-thick PMMA, which is equivalent to a 5.3-cm-
thick breast. The entrance exposure was measured using
an ionization chamber (Radcal 9010 with 6-cc mammo-
probe). The FFDM system used automatic exposure
control to determine the correct technical factors, while a
technique chart was used for the tomosynthesis system.
The FFDM system used 30 kVp, 86 mAs, and rhodium
filtration. The tomosynthesis system technical parameters
were 29 kVp, 62 ms, and aluminum filtration. The
entrance exposure was converted to a mean glandular
dose based on conversion factors estimated by Boone
[26]. The mean glandular dose was 1.70 mGy for the
FFDM system and 1.74 mGy for the tomosynthesis
system [19, 20].
Interpretation of mammography and further work-up
All mammography investigations were directly viewed by
one of seven breast radiologists (624 years of experience,
each viewing more than 1,000 mammograms each year) in
our department. Carestream PACS was used with 2 MP
Barco flat-panel screens. Left and right breasts were scored
separately and classified according to the ACR BIRADS
lexicon criteria [27, 28]. Further workup or strict follow-up
was considered to be necessary when a score of 0, 3, 4, or 5
was given. Further work-up with ultrasound was also done
when indicated because of clinical symptoms such as
palpable mass or pain.
In these cases, the same experienced radiologist who
scored the mammogram performed the breast ultrasound
and FNAB when indicated.
17
Clinical decision-making
The results of clinical examination, radiology, and pathology
were discussed on the same day in a multidisciplinary
meeting (with surgeons, radiologists, pathologists, medical
oncologists, and radiation oncologists) where decisions were
made regarding further diagnostic studies (core biopsy,
MRI), treatment, or follow-up. The results of viewing the
tomosynthesis datatsets were thereby not taken into account.
Viewing tomosynthesis
One to three months after the initial clinical evaluation, all
breast tomosynthesis datasets were separately viewed using
a prototype dedicated workstation (Hologic; with two flat-
panel screens no. E-3621, 3MP), by one dedicated breast
radiologist (H.J.T.) with 24 years of experience with
mammography but none with breast tomosynthesis. The
workstation that was used allowed viewing the datasets of
both breasts, one after the other (CC and MLOviews of one
breast together) with simple post-processingmagnifica-
tion and window-level adjustment. The mammography
views could not be displayed by this workstation. The
radiologist (J.T.) was at that moment blinded to the
mammography views and reports, the radiologic history,
and the pathology outcome but was otherwise offered the
same information available during clinical reading of the
mammograms, i.e., cause for referral and the findings at
clinical investigation. This radiologist had performed the
initial work-up in 39 patients. He therefore was blinded
for the mammography data in most patients. For classifi-
cation, the BI-RADS lexicon for mammography was used,
taking only the breast tomosynthesis investigation into
account. The information (classification) from the tomo-
synthesis studies was used for clinical decisions in only one
case (see below).
Follow-up
All medical records of the patients with an initial diagnosis
of benignancy were viewed after 1824 months, in order to
determine whether breast cancer had been diagnosed in the
meantime.
Statistical analysis
The gold standard for this study was histological verifica-
tion of biopsied lesions (FNAB or core biopsy) or the
results of the follow-up period (as described above). The
sensitivity, specificity, and positive predictive value (PPV)
of both digital mammography and tomosynthesis com-
pared to the gold standard, including Wilson confidence
intervals, were calculated on a per-breast basis. The
difference in the proportions of outcomes between mam-
mography and tomosynthesis was assessed by a two-tailed
z-test (with continuity correction). BI-RADS 0, 3, 4, and 5
were considered positive test results. Because of the fact
that in this specific clinical setting both mammography and
tomosynthesis datasets were viewed only once, no
information on inter- and intraobserver variation could be
obtained.
Results
A total of 1,028 women visited our outpatient breast clinic
between June 2006 and June 2007. Of this group, 513
women underwent both mammography and tomosynthesis.
The mean age was 52 years (range 2992 years). One
hundred thirty-four women (26%) were referred from the
Dutch screening program because of a density or
microcalcifications on the mammogram; 227 cases (44%)
had a palpable mass, pain, or other clinical symptoms; and
152 women (30%) came for a second opinion. The
distribution of the BI-RADS scores at mammography and
tomosynthesis (n=1,026 breasts) is shown in Table 1.
Histopathological proof was available for 344 lesions/
breasts, including all breasts with carcinoma (n=198) and
most benign lesions (n=146, Table 2). Histological proof
was absent for several reasons. In 23 of 92 BI-RADS-3
lesions at mammography, ultrasound showed no abnorm-
alities or detected a simple cyst. Typically, FNAB of BI-
RADS-2 lesions (n=58) demonstrated a cyst, a fibro
adenoma, or normal fibroglandular tissue. In one benign
lesion with BI-RADS-4 at mammography, further work-up
was deferred due to calcifications that appeared unchanged
over several years. In three BI-RADS-0 lesions, work-up
was deferred because of the unchanged appearance of a
density.
A carcinoma was detected in 194 breasts of 189 women.
Five women had bilateral breast cancer. Out of these 194
Table 1 The BI-RADS classification in the whole patient group
(1,026 breasts)
BI-RADS classification Mammography Breast tomosynthesis
No cancer Cancer No cancer Cancer
0 4 1 1 1
1 567 5 589 6
2 146 3 110 2
3 92 22 96 14
4 17 39 30 36
5 2 42 2 53
6 0 86 0 86
Subtotal 828 198 828 198
Overall total 1,026 1,026
18
breasts, 86 tumors in women referred for a second opinion
were known cancers (BI-RADS-6). In the current study,
this group is excluded from further analysis.
During the follow-up period after the initial evaluation
(1824 months), four additional cancers were detected.
One patient was called back after 1 month, when
tomosynthesis demonstrated a BI-RADS-4 lesion that
had not been detected during the initial work-up. One
patient had a 4-mm DCIS, detected when she underwent
bilateral prophylactic mastectomy because of high risk for
development of cancer. Two other women had calcifica-
tions in the breast that were at first considered to be benign
(BI-RADS-3 with tomosynthesis and mammography), but
who underwent stereotaxic biopsy 6 and 12 months after
their first visit to our department, at which point DCIS was
detected.
As a result, 112 cancers were newly detected. In this
group, 8 cancers (7%) were false-negative at tomosynthesis
and would have been missed using breast tomosynthesis
alone (classified BI-RADS1 or 2; Table 3).
Mammography was also false-negative in eight cases
(7%, classified BI-RADS1 or 2; Table 4). The eight false-
negative cancers at mammography were detected using
ultrasound-guided FNAB (n=4 palpable cancers), MRI
(n=2 contra-lateral breast cancers), tomosynthesis (n=1,
recall following assessment of breast tomosynthesis), and
after prophylactic bilateral mastectomy (n=1). In five of
these eight patients, the BI-RADS classification with
tomosynthesis was 4.
In the three other patients, both mammography and
breast tomosynthesis were false-negatives (one invasive
ductal carcinoma, one invasive lobular carcinoma, and one
case of DCIS detected after prophylactic mastectomy).
All clusters of malignant calcifications seen at mam-
mography were also visible at breast tomosynthesis.
Considering BI-RADS-0, 3, 4, and 5 as a positive test
result, the sensitivity of mammography was high (92.9%,
104/112, 95%CI: 86.596.3) and identical to the sensitivity
of tomosynthesis, while the specificity of mammography
(86.1%, 713/828, 95% CI: 83.688.3) was slightly higher
than that of tomosynthesis (84.4%, 699/828, 95% CI: 81.8
86.7) (see Tables 5 and 6). The difference in specificity was
1.7%(asymptotic 95%CI: 1.8 to 5.2), P value = 0.37. The
difference in PPV was 2.9% (asymptotic 95% CI: 6.8 to
12.5), P value =0.61, while the difference in overall
accuracy was 1.5% (asymptotic 95% CI: 1.7 to 4.7),
P value =0.39.
The characteristics of 32 breasts with a benign lesion and
BI-RADS score of 4 or 5 at tomosynthesis are outlined in
Table 7.
Discussion
To our knowledge, this is the first prospective study in
which the sensitivity of breast tomosynthesis alone was
compared with digital mammography alone. In our study,
in women referred to the outpatient clinic of a tertiary
referral hospital, the sensitivity of the techniques was
similar (92.9%), with a specificity of 98.7 and 97.0% for
mammography and breast tomosynthesis, respectively. The
sensitivity of mammography is high in comparison to other
studies [211]. This may be due to the fact that our BI-
RADS-3 findings were considered positive.
The specificity of mammography was somewhat larger
than that of tomosynthesis because tomosynthesis led to
more BI-RADS-4 lesions than BI-RADS-2. This does not
necessarily mean that tomosynthesis will be more specific
Table 3 Cases (n=8) in which breast tomosynthesis was false negative
Case Revision of breast tomosynthesis Mammography Diagnosis
1 Occult BI-RADS-1 IDC
2 Occult BI-RADS-1 ILC
3 Occult BI-RADS-2 DCIS
4 Occult BI-RADS-3, architectural distortion ILC
5 Occult BI-RADS-3, asymmetric dense tissue ILC
6 Calcifications, considered to be benign BI-RADS-3 DCIS
7 Occult, insufficient patient positioning BI-RADS-4 IDC
8 Occult, patient movement BI-RADS-4 IDC
Table 2 Histologic verification of benign lesions
BI-RADS
classification
Mammography Histology
available
Tomosynthesis Histology
available
0 4 1 1 0
1 567 0 589 7
2 146 58 110 47
3 92 69 96 67
4 17 16 30 23
5 2 2 2 2
total 828 146 828 146
19
in this patient category. It is at least in part caused by the
fact that the radiologist who viewed the tomosynthesis
images was blinded to the mammography views and
reports, the radiologic history, and the pathology outcome.
There can also be a difference in the way different
observers used the BI-RADS criteria. The high percentage
of carcinomas in our patient group that were categorized
BI-RADS-3 with mammography (21%) and with tomo-
synthesis (12%) is probably caused by the high prevalence
of cancer in our population.
Table 4 Cases (n=8) where mammography was false negative
Case Revision of mammography Breast tomosynthesis Diagnosis
1 Occult BI-RADS-1 IDC
2 Occult BI-RADS-1 ILC
3 Occult BI-RADS-2 DCIS
4 Occult, visible in retrospect? BI-RADS-4 IDC
5 Occult, visible in retrospect? BI-RADS-4 ILC
6 Visible in retrospect BI-RADS-4 DCIS
7 Visible in retrospect BI-RADS-4 IDC
8 Visible in retrospect BI-RADS-4 IDC
Table 5 Statistical analysis of the tomosynthesis results
Frequency
Percent
Table of test by cancer
cancer test
Truth+ Truth-
Total
Tomo+ 104
11.06
129
13.72
233
24.79
Tomo- 8
0.85
699
74.36
707
75.21
Total 112
11.91
828
88.09
940
100.00
sensitivity 104/112 92.9% 95% CI: 86.5 96.3
specificity 699/828 84.4% 95% CI: 81.8 86.7
PPV 104/233 44.6% 95% CI: 38.4 51.5
NPV 699/707 98.9% 95% CI: 97.8 99.4
Accuracy 803/940 85.4% 95% CI: 83.0 87.5
20
When only BI-RADS-0, 4, or 5 lesions are considered
positive, the sensitivity of mammography is lower at 73%
(which is more in accordance with the existing literature
[211]) and 80% for breast tomosynthesis with a specificity
of 97 and 96%, respectively.
The combination of tomosynthesis with mammography
detected more but not all cancers; five carcinomas were
initially not seen with mammography. Masses in particular
were subjectively more visible with breast tomosynthesis
than with mammography. In retrospect, the initially
undetected lesions could be seen with mammography in
all five cases. The signs were, however, subtle. An example
of one of the cases is shown in Fig. 1. However, with regard
to the diagnosis task, in the setting of our outpatient
clinic for symptomatic patients and screen-detected
abnormalities, the threshold for deciding to perform further
investigation was very low. Hence, four of these five
tumors were detected otherwise (ultrasound or MRI).
Additionally, the concomitant use of tomosynthesis added
to the glandular tissue radiation dose.
In our study we did not compare the performance of the
combined viewing of the tomosynthesis datasets with
mammography compared to mammography alone. We do
not expect that this would have influenced the results; in
three cases, both techniques were negative, also with
Table 6 Statistical analysis of the mammography results
Frequency
Percent
Table of test by cancer
cancer test
Truth+ Truth-
Total
Mammo+ 104
11.06
115
12.23
219
23.30
Mammo- 8
0.85
713
75.85
721
76.70
Total 112
11.91
828
88.09
940
100.00

sensitivity 104/112 92.9% 95% CI: 86.5 96.3
specificity 713/828 86.1% 95% CI: 83.6 88.3
PPV 104/219 47.5% 95% CI: 41.0 54.1
NPV 713/721 98.9% 95% CI: 97.8 99.4
Accuracy 817/940 86.9% 95% CI: 84.6 89.0
Table 7 Benign breast lesions (n=32) where breast tomosynthesis
yielded a BI-RADS score of 4 or 5
Description Number
Microcalcifications subsequently biopsied or unchanged
for several years
18
Architectural distortion, biopsy negative 1
Architectural distortion after surgery, not biopsied 1
Cyst, biopsy negative 2
Microcalcifications and mass; histology: fibroadenoma 3
Suspect mass/density; biopsy negative 6
Others 1
21
retrospective evaluation. It is likely, however, that in the
future, the use of tomosynthesis in combination with
mammography will be investigated.
A limiting factor of this study was the fact that for the
viewing of mammography and tomosynthesis different
display monitors were used. We do not consider it likely,
however, that this has influenced the outcome as both were
fully adjustable for window and level.
Three of the eight cancers that scored BI-RADS-1 or 2 at
breast tomosynthesis were invasive lobular carcinoma
(ILC). This may suggest that tomosynthesis does not lead
to improved detection of ILC compared to mammography.
The relatively high number of benign lesions that were
assigned BI-RADS-4 with breast tomosynthesis is owing
to the fact that the radiologist reading the breast
tomosynthesis examination was blinded to the radiologic
history; a number of these cases showed microcalcifica-
tions that had remained unchanged over several years. In
the past years, several technical innovations have been
introduced in breast radiology, aiming to enhance the
performance of mammography: digital mammography
[1518], contrast-enhanced mammography [16, 20], breast
tomosynthesis [16, 1924], and contrast-enhanced digital
breast tomosynthesis [29]. The primary potential of breast
tomosynthesis is the reduction of the overlap of normal
breast structures with breast abnormalities. This can
potentially lead to better lesion detection and better lesion
delineation but also to a reduction in the recall rate in a
screening population [16, 21].
In recent studies [16, 23, 24], superior visibility of
masses and areas of architectural distortion have been
shown for tomosynthesis. In a group of 40 symptomatic
patients, seven palpable cancers were mammographically
occult. Six of them could be detected using breast
tomosynthesis [16]. In another study [24], the BI-RADS
classification was upgraded in a significant number of
patients. In a study by Rafferty [16], the visualization of
microcalcifications was better with mammography than
with tomosynthesis probably because of the cross-sectional
nature of breast tomosynthesis; existing microcalcifications
are visualized in different tomosynthesis planes. This
suggests that breast tomosynthesis and mammography may
best be used in a complementary way. We will investigate
this in a future study. Breast tomosynthesis may also play a
role in the better delineation of breast tumors by reducing
overlap of confounding normal structures, potentially
leading to better discrimination between benign and
malignant lesions. This was also investigated by Rafferty
[16]. In our study we found delineation of lesions indeed
subjectively better, especially in benign lesions, which
may theoretically obviate the need for subsequent ultra-
sonography. On the other hand, some malignant tumors
also have sharp boundaries [30]. Hence, improved visual-
ization of lesion boundaries can potentially lead to a false
benign diagnosis.
Initially it was expected that the three-dimensional
information from the breast tomosynthesis acquisition
would make it possible to acquire only one projection
image (MLO). The pilot study by Rafferty and colleagues
[16] with breast tomosynthesis done in two projections in
34 lesions demonstrated better visibility of the lesion in one
of the projections in 12 of the cases. In our patient group
the lesions were generally equally well visualized in both
projections. Causes for inadequate visualization can be
patient motion, especially in the MLO projection, probably
caused by the relatively long acquisition time combined
with insufficient compression, but also by incomplete
breast tissue display. In our experience, both projections
should be made and technicians have to be instructed very
well, so that compression will be sufficient. In the near
future, the expected combination of breast tomosynthesis
and mammography in one acquisition unit combined with
Fig. 1 Case 1. a MLO projection (mammography), classified BI-
RADS-1. Carcinoma detected with ultrasound. b CC projection
(mammography), classified BI-RADS-1. c One slice of CC projec-
tion (tomosynthesis), classified BI-RADS-4. d Magnification of one
slice of CC projection (tomosynthesis), classified BI-RADS-4
22
shorter acquisition time will facilitate optimization of the
technique. Displaying both modalities on one work station
(preferably with 5 MP screens) may potentially lead to a
better performance.
Conclusion
Tomosynthesis can be used as an additional technique to
mammography in patients referred with an abnormal
screening mammogram or with clinical symptoms. Addi-
tional lesions detected by tomosynthesis, however, are also
likely to be detected by other techniques used in the clinical
work-up of these patients. Therefore, the role of tomo-
synthesis is not yet established.
Acknowledgements This study was supported by a grant from
Hologic Inc., Bedford, MA. We are grateful to Angelique Schlief for
preparing the database and to Loren Niklason (Hologic) for critically
proof-reading the manuscript.
Conflict of interest declared Grant From Hologic Inc. to H.J.
Teertstra.
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