Key words mammography - breast ultrasound - complementary breast diagnostics
Introduction
Multimodal imaging continues to be standard for the diagnosis of malignant tumours
of the breast. There are however various problems, discussion points and challenges
regarding the different imaging modalities (mammography/tomosynthesis, ultrasound
and MRI) in their individual areas of clinical application. In the screening domain,
where mammography is used exclusively [1 ], the high diagnosis rate of non-lethal tumours (overdiagnosis) is cited [2 ], [3 ]. And tumours that are missed on mammogram alone, e.g. due to high mammographic density,
are also a problem (underdiagnosis) [4 ], [5 ]. In the diagnostic domain, where complementary breast imaging with both ultrasound
and mammography is standard [6 ], spatial mapping requires further optimisation.
Current strategies to optimise diagnostic imaging include improving the quality of
the individual modalities, integrating computer-assisted evaluation [7 ], focusing on three-dimensional modalities [8 ] and combining the different modalities (fusion) [9 ], [10 ]. Since the development of three-dimensional mammography (tomosynthesis) and ultrasound
(automated breast ultrasound) interest has especially focused on fusion devices, as
the characterisation of breast lesions can be difficult when these modalities are
used independently. The error rate on correlation between lesions detected on mammogram
compared to hand-held ultrasound is around 10% [11 ]. The combination of modalities in a single continuous examination of the immobilised
breast could help to reduce these problems.
The fusion approach to improve breast diagnostic imaging whereby multiple imaging
modalities such as mammography, breast ultrasound, MRI and tomosynthesis are combined
– the strengths of the one compensating for the weaknesses of the other – is not new
[10 ], [12 ], [13 ], [14 ]. Combining modalities, however, presents new challenges such as how to perform multiple
imaging procedures on the compressed breast in series or simultaneously without changing
its position. This is essential for precise localisation of regions of interest (ROI).
Combined imaging is currently not yet part of routine clinical practice due to an
unfavourable cost-benefit ratio and a lack of technical feasibility [10 ].
In contrast to previous studies in which principally analogue images were acquired
[12 ], [15 ], [16 ] this study was based on digital mammography and 3D ultrasound examination.
The aim was to validate a functional fusion prototype using a small number of mastectomy
specimens.
Methods
Development of a novel gauze compression device
A compression device for breast immobilisation is an essential requirement for a combination
unit required to perform both ultrasound and mammography/tomosynthesis in a single
examination session. The mammogram is performed according to radiological standards
[17 ] as stipulated in the mammography screening guidelines [6 ], [18 ]. X-rays and ultrasound waves should not be impeded and the quality of images not
compromised. Breast coverage should be as complete as possible for both the mammogram
and ultrasound examination components. A newly developed compression device consisting
of an elastic gauze mounted onto a frame provided the required breast compression
(up to 100 Newton [N] [19 ]) ([Fig. 1 ]).
Fig. 1 The ultrasound probe – taken from the ABVS ultrasound machine – moves over the compressed
(elastic gauze) breast phantom.
Integration into the mammography unit
The MAMMOMAT Inspiration served as the basic unit. Ultrasound imaging was carried
out by a probe from an Acuson S2000 ABVS machine (both Siemens Healthcare Ltd). The
ultrasound probe-gauze unit is flanged-mounted to the mammography unit via a horizontal
lowerable holder instead of the standard compression plate ([Fig. 2 ]). The entire unit can hereby be moved up or down enabling variation of the compression
force applied to the breast. The prototype described here is a research tool and is
not commercially available.
Fig. 2 a The illustration shows the prototype attached to the Siemens MAMMOMAT Inspiration.
The automatic, adjustable ultrasound probe taken from a Siemens S2000 ABVS system
is seen mounted on a threaded rod (left in picture) up against the transparent gauze
that provides breast compression. b Schematic representation of the integrated mobile ultrasound probe-gauze unit.
Specimens
The mastectomy specimens were obtained during the iMODE-B study (Imaging and Molecular
Detection study Breast). All the patients were fully informed and gave written consent
to study inclusion. The study was approved by the medical faculty ethics commission
of the Friedrich-Alexander University, Erlangen-Nürnberg.
Fusion prototype imaging was performed on unfixed abladates in the Erlangen University
Hospital radiology institute, department of gynaecological radiology. Thereafter the
abladates were passed on to the hospitalʼs pathology institute for evaluation of resection
margins and histological analysis.
Imaging procedure
Each mastectomy specimen was x-rayed twice, first using the standard compression plate
and then the newly developed compression gauze. For the latter the breast is compressed
to the required thickness with up to 100 N by the taut elastic gauze fixed to the
underside of the compression frame. This is equivalent to the same pressure applied
during conventional mammography [19 ]. The compression applied by the gauze can be adjusted according to the individual
breast shape allowing the pressure to be evenly distributed. A craniocaudal (CC) mammogram
is performed with the mammography unit using a standard protocol. During x-ray imaging
the ultrasound probe remains outside the field of radiation at the edge of the compression
plate. Ultrasound imaging then follows without any repositioning of the already compressed
breast. The probe frequency can be adjusted to suit individual circumstances. After
completion of the mammogram conventional ultrasound gel is applied to the gauze ahead
of the probe. The probe, attached to a threaded rod, then automatically travels out
from right to left over the compressed breast. The ultrasound machineʼs (Siemens Acuson
S2000 ABVS) standard software is used for 3D image reconstruction. Finally the gauze
is replaced by the conventional compression plate and an additional image obtained
for comparison. The gauze was replaced after each examination for hygienic reasons.
Quality evaluation
Each pair of images (gauze compression and conventional compression plate) was assessed
independently in randomised order by two radiologists who were blinded to patient
details. Image pairs were evaluated for quality by internal comparison. In addition
they were assessed for the detection of microcalcification, macrocalcification and
masses, all of which are regarded as possible correlates of malignant or premalignant
lesions [20 ]. The case series analysis was purely descriptive at the level of the depiction of
findings in each specimen. The image pairs are shown in [Fig. 3 ].
Fig. 3 The illustration shows CC images of an abladate; on the right with conventional compression
(mammography unit), on the left with compression gauze.
Results
Combined imaging with mammography and automated ultrasound was successfully performed
on all 5 mastectomy specimens.
Patient characteristics
Patient characteristics are listed in [Table 1 ]. Various clinical scenarios were chosen in order to provide as comprehensive an
assessment of image quality as possible. Included were: a case of a previously operated
breast (patient 1); a case of DCIS (patient 2); a case of breast carcinoma following
neoadjuvant chemotherapy (patient 4); and one case each of unifocal (patient 3) and
multifocal (patient 5) breast carcinoma.
Table 1 Patient characteristics. Clinical data and the compression force in Newton required
for an adequate mammogram are listed for each of the 5 patients.
Patients
Age (years)
pT
Weight of abladate (g)
Size of findings (cm)
Compression force (N) plate/gauze
1
58
pTis
551
–
97.6/88.8
2
71
pTis
372.4
8.9
48.2/52.2
3
50
pT1c
249.5
1.6
26.7/32.5
4
50
ypT2
408
2.5
39.7/32.8
5
81
pT2m
767
4.6
19.4/21.9
Evaluation of feasibility
Positioning and compression of the breast, the mammogram and ultrasound examinations
were all unproblematic. Compression and mammography were not more time-consuming or
labour intensive than conventional mammography. The required pressure for breast compression
was achieved without difficulty. The pressure actually needed was significantly below
the maximum possible pressure in 4 of the 5 cases ([Table 1 ]). Automated ultrasound examination and changing of the compression gauze were also
unproblematic.
Evaluation of the compression procedure
Using the gauze was unproblematic, both for breast compression and specimen alignment.
The degree of compression necessary for a high quality mammogram was achieved in every
case. The actually required compression force for each individual case did not differ
significantly between the two methods (see [Table 1 ]).
Image quality when using compression gauze compared to conventional compression plate
The quality of the two imaging methods was found to be comparable using the above
mentioned comparison procedure. On comparison of mastectomy specimen image pairs one
radiologist considered them identical in all 5 cases. In 2 cases the second radiologist
rated the quality slightly better for the mammograms with conventional compression;
the remaining 3 cases received equal ratings. The ability to detect microcalcification,
macrocalcification and masses was identical for the two compression methods. Results
are summarised in [Tables 2 ] and [3 ].
Table 2 Direct comparison of images with compression gauze and compression plate. Each letter
represents a rating by one of the radiologists.
Patient
1
2
3
4
5
1 = Gauze image much better; 2 = gauze image somewhat better; 3 = no difference; 4
= compression plate image somewhat better; 5 = compression plate image much better.
A: selection radiologist 1, B: selection radiologist 2
1
A
B
2
A/B
3
A/B
4
A
B
5
A/B
Table 3 Rating of compression methods (compression plate and compression gauze) for ability
to detect microcalcification, macrocalcification and mass lesions. Each letter represents
a rating by one of the radiologists.
Patient
Tumour visible (yes/no)
Microcalcification visible (yes/no)
Macrocalcification visible (yes/no)
A: selection radiologist 1, B: selection radiologist 2
1: Gauze
n. a.
A/B
1: Compression plate
A/B
2: Gauze
A/B
A/B
A/B
2: Compression plate
A/B
A/B
A/B
3: Gauze
A/B
A/B
3: Compression plate
A/B
A/B
4: Gauze
A/B
A/B
A/B
4: Compression plate
A/B
A/B
X/X
5: Gauze
A/B
A/B
5: Compression plate
A/B
A/B
Evaluation of ultrasound images
Automated ultrasound of the compressed breast could be performed quickly (approx.
70 sec) through the gauze. When compared to the mammogram ultrasound provided almost
complete coverage of the specimen. A narrow band of tissue including the nipple region
and skin was not covered by the ultrasound examination due to the compressed breastʼs
convex form. Reconstruction of a 3D picture from the individual images was possible.
[Fig. 4 ] shows the mammogram (right), the sagittal automated ultrasound image (below) and
the 3D reconstruction (left).
Fig. 4 The illustration shows the mammogram of a patient with a cT2 invasive breast carcinoma,
right; below, the ROI from the practically simultaneously performed ultrasound examination;
left, 3D breast reconstruction of the ROI.
Discussion
This fusion prototype consisting of a mammography unit and a standard 3D ultrasound
probe enables the combination of mammography and ultrasound examination by a single
machine. Both imaging modalities are performed on the immobilised breast during one
examination procedure without the position or form of the breast being changed.
Advantages are that the patient does not have to change position for the two images,
both images are performed practically at the same time, and that the breast remains
in an identically compressed condition for both images. The problems of position change
and biological factors such as cyclical fibrocystic changes are therefore much less
significant [21 ]. This has improved suboptimal correlation of findings between the individual modalities
[11 ].
As has been shown in other studies with similar forms of compression [13 ] the compression gauze did not reduce the quality of mastectomy specimen images.
This suggests that the image quality of mammograms performed on patients using this
method will be just as good, so that appropriate clinical studies can now be planned.
This prototype allows automated ultrasound imaging and 3D reconstruction. The extent
of breast coverage however does not yet allow detailed assessment of the nipple or
subcutaneous regions, a problem also experienced by other study groups [21 ]. Current research is focusing on optimising ultrasound coverage of the whole breast.
Although we did not specifically evaluate the quality of 3D ultrasound in this study,
a strong impression was gained that – apart from coverage of the above mentioned regions
– there were no qualitative deficits.
This study has shown that the fusion of these two modalities is also possible with
digital technology. Although the strength of a study with only five specimens is low,
the automatic correlation of lesion localisation between the two modalities appeared
to be very accurate.
These findings are still of limited significance, firstly due to the low number of
examined specimens and secondly due to a lack of implementation in routine clinical
practice. A definitive evaluation of 3D ultrasound image quality is also still lacking.
Nevertheless these results should prompt further study and improvement of this technology.
Future studies should assess the feasibility of the method with respect to patient
pain perception, duration of examination and image analysability. Ultrasound coverage
of the breast through modification of the ultrasound probe and gauze, as well as automated
spatial mapping should be further studied and optimised. Lastly, the learning curve
associated with this technology also requires study.
Conclusion
The fusion of an automated 3D ultrasound machine with a standard mammography unit
delivers mammogram images of comparable quality to conventional mammograms as demonstrated
on a few mastectomy specimens. In addition, this prototype allows simultaneous ultrasound
– a second imaging modality as part of complementary breast diagnostics – with no
significant increase in examination time or personel requirements.
