John M.
Lewin, MD Dual-Energy Contrast-
Radiology
Pamela K. Isaacs, DO
Virginia Vance, RN
Fred J. Larke, MS
Index terms:
Breast radiography, comparative
studies, 00.119
Breast radiography, technology,
00.119
Published online before print
10.1148/radiol.2291021276
Radiology 2003; 229:261–268
Abbreviations:
DCIS ⫽ ductal carcinoma in situ
DSM ⫽ digital subtraction
mammography
1
From the Department of Radiology,
University of Colorado Health Sciences
Center, Denver; and Department of Ra-
diology, University of Colorado Hospital
Breast Center, Rm 3140A/Mailstop
F724, 1635 N Ursula St, Aurora, CO
80010. From the 2001 RSNA scientific
assembly. Received October 3, 2002; re-
vision requested November 27; final re-
vision received March 17, 2003; ac-
cepted April 7. Supported by a grant
from the Susan G. Komen Breast Cancer
Foundation. Address correspondence
to J.M.L. (e-mail: john.lewin@uchsc.edu).
Author contributions:
Guarantor of integrity of entire study,
J.M.L.; study concepts and design,
J.M.L.; literature research, J.M.L.; clinical
studies, J.M.L., V.V., P.K.I.; experimental
studies, J.M.L., F.J.L.; data acquisition,
J.M.L., V.V.; data analysis/interpretation,
J.M.L.; statistical analysis, J.M.L.; manu-
script preparation, definition of intellec-
tual content, and editing, J.M.L.; manu-
script revision/review and final version
approval, all authors
©
RSNA, 2003
enhanced Digital
Subtraction Mammography:
Feasibility1
A technique for demonstrating
breast cancers, dual-energy contrast
agent– enhanced digital subtraction
mammography, was performed in
26 subjects with mammographic or
clinical findings that warranted bi-
opsy. The technique consists of high-
energy and low-energy digital mam-
mography after administration of
iodinated contrast agent. Weighted
subtraction of the logarithmic trans-
form of these images is then per-
formed to obtain an image that pref-
erentially shows iodine. Of the 26
subjects, 13 had invasive cancers.
Eleven of these tumors enhanced
strongly, one enhanced moderately,
and one enhanced weakly. The duct
in one patient with ductal carcinoma
in situ was weakly enhancing. In the
other 12 patients, benign tissue en-
hanced diffusely in two and weakly
focally in two. These results indicate
that the technique is feasible and
worthy of further study.
©
RSNA, 2003
At mammography, 10%–20% of breast
cancers (1,2), including at least 9% of
those already palpable (3), are not de-
picted. It has been hoped that full-field
digital mammography, because of supe-
rior contrast resolution, will prove supe-
rior to standard screen-film mammogra-
phy in the detection of breast cancers.
This hope, unfortunately, was not borne
out in one clinical study (4). Techniques
are sought that make use of the technical
properties of full-field digital mammog-
raphy to find more cancers. One pro-
posed idea is to use an intravenous iodin-
ated contrast agent to attempt to
enhance cancers that would otherwise be
mammographically occult. Digital sub-
traction angiography of the breast with
fluoroscopic equipment was performed
for evaluation of breast tumors almost 20
years ago (5) but did not prove to be
clinically useful. Breast cancers have
been shown to enhance with iodinated
contrast agents at computed tomography
(CT) (6,7) and with gadolinium-based
contrast agents at magnetic resonance
(MR) imaging (8 –10).
There are difficulties inherent in this
approach. The contrast resolution of full-
field digital mammography, although su-
perior to that of screen-film mammogra-
phy, is far less than that of CT or MR
imaging. Additionally, the breast com-
pression used for mammography creates
an external pressure that is greater than
the venous pressure. Thus, venous out-
flow is restricted, which potentially de-
creases delivery of the contrast agent to
the tissues. Suboptimal tissue enhance-
ment while the breast is under compres-
sion precludes the use of compression if
the technique requires subtraction of pre-
contrast from postcontrast images. This
is done in breast MR imaging because the
position of the breast cannot be repro-
duced adequately if compression is re-
leased and then reapplied.
Since June 2000, we have studied tech-
niques for performing contrast agent– en-
hanced digital subtraction mammogra-
phy (DSM). Dual-energy subtraction is
used in one of these techniques. Thus,
the purpose of our study was to evaluate
a technique we developed, dual-energy
contrast-enhanced DSM, for use in dem-
onstrating breast cancers.
Materials and Methods
Patients
From November 2000 to January 2002,
patients with mammographically occult
or mammographically visible lesions that
261
 TABLE 1
Malignant Lesions at Dual-Energy Contrast-enhanced Digital Subtraction Mammography
Subjective Contrast-
Patient Size Detected at Enhancement to-Noise
No. Pathologic Finding (mm)* Palpable Mammography Mammographic Finding Score† Ratio‡
Radiology

1 Invasive lobular carcinoma 94 Yes No No finding Moderate NA§

2 Invasive lobular carcinoma, DCIS 12 Yes No No finding Strong 3.4
3 Invasive ductal carcinoma 20 Yes No No finding Strong 4.1
5 Invasive ductal carcinoma, DCIS 30 Yes Yes Mass Weak 㛳 1.9㛳
6 Invasive ductal carcinoma 11 No Yes Mass Strong 2.5
10 Invasive ductal carcinoma, DCIS 43# Yes Yes Microcalcifications Moderate 2.8
11 Tubular carcinoma 5 No No No finding Strong 4.1
12 DCIS 31# No Yes Microcalcifications Possible 1.2
14 Invasive ductal carcinoma, DCIS 12 No No No finding Weak** 1.2**
15 Invasive ductal carcinoma, DCIS 18 No Yes Mass Strong 2.2
21 Invasive ductal carcinoma 20 Yes Yes Mass Strong 2.8
22 Invasive ductal carcinoma 20 No Yes Architectural distortion Strong 2.6
23 Invasive ductal carcinoma, DCIS 28 No Yes Microcalcifications, mass Moderate 2.5
24 Invasive ductal carcinoma 23 No Yes Mass Strong 2.4
* Longest dimension determined at pathologic examination, unless specified otherwise.
† Rated by blinded observer.
‡ Between the lesion and adjacent tissue.
§ NA ⫽ not applicable. Contrast-to-noise ratio could not be measured because of the infiltrating nature of the tumor with no discernible mass.
㛳 Only about 60 mL of contrast agent was injected because an intravenous tubing connection was lost.
# Maximal extent of calcification, in ductal orientation.
** Injection rate of 2 mL/sec.

required biopsy or that were believed

subjectively by an experienced breast im-
ager (J.M.L.) to have a 50% or greater
probability of being malignant were of-
fered enrollment in this study. Women
with contraindications to receiving an io-
dinated contrast agent were excluded.
Each woman gave written informed con-
sent. The protocol and consent form
were approved by the Colorado Multiple
Institution Review Board.
Twenty-six women (age range, 33– 84
years; mean age, 51 years) were enrolled.
A 27th patient, who enrolled in the study
on the basis of adenocarcinoma of un-
known origin in a supraclavicular lymph
node, was later excluded because the en-
rollment criteria were not met: No pri-
Figure 1. X-ray spectra calculated for high- and low-energy beams.
mary lesion was found. All enrolled sub-
Each curve is scaled to represent exposure through a 4.5-cm-thick
jects completed the study. Twenty-four 50% glandular–50% fat breast. High-energy parameters include 44
subjects were enrolled on the basis of le- kVp, rhodium anode, 0.025-mm-thick rhodium and 8-mm-thick alu-
sions that were mammographically de- minum filters, and 200 mAs. Low-energy parameters include 30 kVp,
tected (n ⫽ 16), mammographically oc- molybdenum anode, 0.03-mm-thick molybdenum filter, and 140
cult but palpable (n ⫽ 5), or both mAs. The k edge of iodine, at 33.2 keV, is marked by a dashed line.
(Modeling program courtesy of General Electric Corporate Research
mammographically visible and palpable
and Development, Niskayuna, NY.)
(n ⫽ 3). Two additional subjects had le-
sions that were neither mammographi-
cally visible nor palpable. The lesion in
patient 6 was found incidentally during visible as a hypoechoic focus at US was follow-up at 6 months or later with no
ultrasonography (US) for a nearby palpa- canceled when the lesion disappeared at evidence of malignancy.
ble abnormality. The lesion in patient 14 both palpation and US. Findings at
was found at MR imaging performed be- 1-year follow-up physical examination
Image Acquisition
cause of cancer in an ipsilateral axillary and mammography showed no sign of
lymph node. disease. In all patients with cancer, core The examination for each patient in-
The diagnosis was established at core biopsy was followed by surgical excision. cluded low- and high-energy exposures
biopsy in all but one patient. In that pa- All patients with benign biopsy results during a single breast compression in the
tient, biopsy of a palpable lesion that was underwent clinical and mammographic mediolateral oblique projection. The breast

262 䡠 Radiology 䡠 October 2003 Lewin et al

 TABLE 2
Benign Lesions at Dual-Energy Contrast-enhanced Digital Subtraction Mammography
Subjective Contrast-
Patient Size Detected at Mammographic Enhancement to-Noise
No. Pathologic Finding (mm)* Palpable Mammography Finding Score† Ratio‡
Radiology

4 Focal fibrosis 22 No Yes Density None 0.0

7 Atypical lobular hyperplasia 6 No Yes Microcalcifications None ⫺0.2
8 Apocrine metaplasia 6 No Yes Density None ⫺0.1
9 Fibroadenoma, ductal hyperplasia 11 No Yes Microcalcifications None 0.1
(usual type)
13 Ductal hyperplasia (usual type), 11 No Yes Mass None 0.2
apocrine metaplasia
16 Ductal hyperplasia (usual type), 8 No Yes Microcalcifications None§ 0.2
fibroadenoma
17 Focal fibrosis 16 No Yes Microcalcifications None§ 0.3
18 Atypical ductal hyperplasia 10 No Yes Microcalcifications Weak 0.7
19 Fibrocystic change 20 Yes No No mass Weak 0.6
20 Sclerosing adenosis 6 No Yes Microcalcifications None ⫺0.1
25 No biopsy㛳 20 Yes No No mass None 0.2
26 Atypical lobular hyperplasia 35 No Yes Microcalcifications None 0.1
* Longest dimension determined at mammography if depicted or palpation if mammographically occult.
† Rated by blinded observer.
‡ Between the lesion and adjacent tissue.
§ Mild diffuse enhancement.
㛳 Biopsy was canceled because of the disappearance of the palpable and sonographic finding. No evidence of disease at 12-month follow-up.

Figure 2. Patient 2. Invasive lobular carcinoma (12-mm diameter). Metal bead marks the palpable abnormality. (a) Mediolateral oblique
mammogram is normal. (b) Precontrast dual-energy DSM image shows elimination of normal breast parenchyma. (c) Enhanced dual-energy DSM
image shows the cancer as a round enhancing mass (arrow) in the superior part of breast.

Volume 229 䡠 Number 1 Digital Subtraction Mammography 䡠 263

 was then released from compression, and
the contrast agent was administered. Af-
ter a delay of about 150 seconds, the
breast was compressed again, and the
low- and high-energy exposures were re-
peated. From these images, pre- and post-
Radiology

contrast dual-energy images were cre-

ated.
Images were acquired with a full-field
digital mammography unit (Senographe
2000D; GE Medical Systems, Milwaukee,
Wis). This unit allows a choice of either
molybdenum or rhodium target materi-
als and internal molybdenum (0.03-mm)
or rhodium (0.025-mm) filters. To deter-
mine reasonable high- and low-energy
techniques, an iodine-containing phan-
tom (Nuclear Associates, Hicksville, NY)
was covered with BR-12 breast-equiva-
lent material of varying thicknesses and
imaged at selected x-ray beam voltages
(low-energy beam, 22–33 kVp; high-
energy beam, 44 – 49 kVp). Only the rho-
dium target–rhodium filter combination
was tested for the high-energy beam be-
cause this combination allows the hard-
est beam with the least tube heating.
For the high-energy beam, an alumi-
num filter with varying thicknesses
(range, 1– 8 mm) was placed in the beam. Figure 3. Patient 6. Invasive ductal carcinoma (11-mm diameter). (a) Mediolateral oblique
For the low-energy beam, the combina- mammogram shows possible spiculated mass (arrow). (b) Dual-energy enhanced DSM image
tions of molybdenum target with molyb- shows the cancer as an enhancing mass with definite spiculations (arrow).
denum filter and rhodium target with
rhodium filter were tested. The tech-
niques for low- and high-energy acquisi-
tions were chosen to maximize and min- a 50% glandular–50% fat breast with injection rate of 2 mL/sec. The breast was
imize, respectively, the ratio of the compressed thickness of 4.5 cm, the dose not compressed during injection. All 26
attenuation of breast-equivalent material was calculated to be 0.7 mGy above that subjects tolerated the contrast agent ad-
to that of iodine on the phantom images. needed for conventional mammography. ministration well without complaint.
Results of these preliminary studies
Contrast Agent Administration Image Processing and Evaluation
showed that a high-energy technique of
44 kVp with 8 mm of aluminum would The contrast agent (iohexol [100 mL, Custom image processing software was
work well. Results were equivalent with with 350 mg of iodine per milliliter], Om- written (J.M.L.) in interactive data lan-
several low-energy techniques, presum- nipaque 350; Amersham Health, Prince- guage (IDL; Research Systems, Boulder,
ably because of the dominance of the k␣ ton, NJ) was administered with a me- Colo). To create a dual-energy image,
and k␤ peaks of the target material, which chanical power injector (Vistron CT; weighted subtraction of the logarithm of
are in the range of 18 –22 keV, which is Medrad, Indianola, Pa) via a short 20- the low-energy image from that of the
far from the k edge of iodine (33.2 keV). gauge intravenous catheter placed in an high-energy image was performed. The
For the present study, most low-energy antecubital or forearm vein, at a rate be- weighting factor for the precontrast im-
images were acquired at 30 kVp with a tween 4 and 5 mL/sec. The injection rate ages was chosen as the value that elimi-
molybdenum target–molybdenum filter was governed by a subjective assessment nated the visibility of changes in the
combination (patients 1–9) or at 33 kVp of the quality of the venous access. In thickness of breast-equivalent material
with a rhodium target–rhodium filter patient 5, contrast agent administration on a phantom made of overlapping lay-
combination (patients 10 –26). Mean had to be stopped twice because of a loss ers of the material. The optimal weight-
time between exposures was 30 seconds of the connection between the tubing ing factor is dependent on the x-ray
(range, 24 –50 seconds). During this time, and the intravenous catheter. Because of beam voltage, target, and filter of the im-
the first image was acquired and dis- the time required to reestablish the con- age pair but not on the tube current and
played, the techniques were changed, nection in this case, only 60 mL of con- exposure time. A weighting factor of 0.20
and the additional aluminum filter was trast agent was administered during 3 was used with a low-energy technique of
placed in the x-ray beam. Energy spectra minutes. In patient 14, rather than sub- 30 kVp with molybdenum target and
calculated for the beams are shown in ject the patient to placement of a second molybdenum filter and was 0.26 with 33
Figure 1. Half-value layers for the low- intravenous catheter, we used an intrave- kVp with rhodium target and rhodium
and high-energy beams were 0.39 and nous catheter that was previously placed filter. A 4 ⫻ 4 boxcar filter was applied to
3.07 mm of aluminum, respectively. For in a hand vein for MR imaging, with an each image for noise reduction.

264 䡠 Radiology 䡠 October 2003 Lewin et al

 Figure 4. Patient 10. Invasive ductal carci-
noma and DCIS. (a) Mediolateral oblique
mammogram shows grouped microcalcifica-
tions in the breast (arrows) and in a lymph
node (arrowhead). Enhancement is barely per-
Radiology

ceptible on postcontrast (b) low-energy and

(c) high-energy images. (d) Subtracted dual-
energy enhanced DSM image shows the inva-
sive component as enhancing lesions (black
arrows), but there is no definite enhancement
around grouped calcifications in the posterior
breast (white arrow). The malignant lymph
node (arrowhead) also enhanced.

Contrast-to-noise ratios were calcu-

lated. A region of interest was drawn
manually (J.M.L.) around the lesion for
comparison with the surrounding tissue
within a 9-mm radius of the margin, ex-
cluding the 3 mm immediately adjacent
to the region of interest. The average of
three measurements is reported. Subjec-
tive judgement of lesion enhancement—
with the scale of strong, moderate, weak,
possible, and none—was performed (P.K.I.)
with the clinical full-field digital mammog-
raphy review workstation with dual 2.0 ⫻
2.5-megapixel monitors. The reader was
not familiar with the cases, was blinded
to the pathologic result, and did not have
access to the raw images or the standard
mammograms.

Results
Tables 1 and 2 give the details for each
lesion, the protocol used, the injection
rate used, and the results of dual-energy
enhanced DSM. Thirteen subjects had in-
vasive carcinomas, and one subject had
ductal carcinoma in situ (DCIS). Three of
the cancers were palpable but mammo-
graphically occult, seven were mammo-
graphically visible but not palpable, two
were both palpable and mammographi-
cally visible, and two were neither palpa-
ble nor mammographically visible. Be-
nign lesions included focal fibrosis and a
variety of usual and atypical proliferative
changes. The patients are separated into
benign and malignant categories in these
tables. The patient number indicates the
order in which each subject was enrolled.
Eleven of the invasive cancers en-
hanced strongly and had contrast-to-
noise ratios above 2.0 (Figs 2, 3). The
other two invasive cancers enhanced
weakly. The subjective judgement of le-
sion enhancement generally agreed with
the contrast-to-noise ratio.
In patient 12, with pure DCIS, the duct
was faintly enhancing. In patient 10,
with both invasive and in situ carci-

Volume 229 䡠 Number 1 Digital Subtraction Mammography 䡠 265

Radiology
Figure 5. Patient 18. Benign tissue at remote lumpectomy site. Results of biopsy of new calcifications in the area showed atypical ductal
hyperplasia. (a) Mediolateral oblique mammogram shows new grouped calcifications (arrow). (b) Precontrast dual-energy DSM subtraction image
shows subtraction of breast tissue. (c) Enhanced dual-energy DSM image shows faint enhancement of the area around the lumpectomy site
(arrowheads).
noma, strong enhancement of the inva-
sive component was seen but not en-
hancement around the calcifications
associated with the DCIS (Fig 4).
In two patients with benign findings,
areas of focal non-masslike enhancement
were seen. These findings are potentially
false-positive. In patient 18, the lesion
was in an area of atypical ductal hyper-
plasia that surrounded the site of previ-
ous lumpectomy (Fig 5), while that in
patient 19 was in an area of fibrocystic
change. In two other patients with be-
nign findings, diffuse enhancement of
normal breast tissue was seen. In patient
11, with cancer, diffuse enhancement of
the normal parenchyma was seen in ad-
dition to enhancement of the cancer as a
5-mm-diameter mass (Fig 6).
Discussion
In this small study, dual-energy en-
hanced DSM demonstrated most of the
266 䡠 Radiology 䡠 October 2003
known cancers, including those that
were visible at standard mammography
and those that were not (as well as a few
false-positive findings). The study was
not intended to be a definitive test of
enhanced DSM but rather a demonstra-
tion of its feasibility and potential. To
improve our chances of success, we opti-
mized the x-ray beam energy, incorpo-
rated power injection at a high rate, and
eliminated breast compression during in-
jection by means of dual-energy subtrac-
tion. Dual energy allowed full compres-
sion during imaging, which increased the
morphologic definition of the lesion. Ad-
ditionally, compared with temporal sub-
traction, dual-energy subtraction increases
the options for imaging. With temporal
subtraction, for example, multiple views
cannot be obtained with a single injec-
tion. Because dual energy does not re-
quire the matching of pre- and postcon-
trast views, images can be obtained in
multiple projections, which allows local-
ization of any enhancing lesion.
Enhanced DSM is similar in concept to
enhanced breast MR imaging and could
potentially be applicable in situations in
which MR imaging is currently used.
Such situations include detection of a pri-
mary breast cancer in a woman with a
positive axillary lymph node and deter-
mination of the extent of disease in cases
of known cancer, as well as problem solv-
ing in cases of mammographic findings
that were not depicted in additional
mammograms or US scans.
It remains to be seen whether the sen-
sitivity to cancer is as high for enhanced
DSM as it is for MR imaging, which has
been shown to have a very high sensitiv-
ity (8 –10). Both techniques make use of
the same property of tumor angiogenesis,
which causes cancers to take up contrast
agent faster and to a greater degree than
do normal tissue or benign masses be-
cause of denser capillaries that are also
Lewin et al
Radiology

Figure 6. Patient 11. Mammographically and clinically occult tubular carcinoma (5-mm diameter). (a) Mediolateral oblique mammogram is
normal. Metal bead marks a palpable abnormality with the pathologic finding of fibroadenoma. (b) Precontrast dual-energy DSM subtraction image
shows subtraction of breast tissue. (c) Enhanced dual-energy DSM image shows enhancement of the cancer (arrow) and diffuse enhancement of
normal tissue.

abnormally “leaky” (11). Because of its
higher contrast resolution, MR imaging is
probably more sensitive to contrast en-
hancement than is enhanced DSM, but
the degree to which that translates into
higher sensitivity for cancer detection is
unknown. One drawback of MR imaging
is that its high sensitivity to contrast
agent uptake causes it to be plagued by
numerous false-positive foci of enhance-
ment. MR imaging also has relatively
limited sensitivity to DCIS, which is de-
picted as microcalcifications at mam-
mography (12). Enhanced DSM was 83%
specific in this study, and the low-energy
source image showed microcalcifications,
which could be used in the diagnosis of
DCIS.
Findings with MR imaging suggest that
morphologic features (ie, shape and mar-
gin) help differentiate benign from ma-
lignant enhancing areas (13). Because en-
hanced DSM allows a higher spatial
resolution than that with MR imaging,
differentiation of benign from malignant
morphologic features at enhanced DSM
should be easier. Enhancement kinetics,
also used for differentiating benign from
malignant lesions at MR imaging (14),
can be determined at enhanced DSM
with serial imaging. Because whole-
breast images can be acquired more rap-
idly than with most MR imaging se-
quences, kinetic information could be
determined with greater precision. Un-
like MR imaging, however, each image
has a penalty of additional radiation. En-
hanced DSM should be less expensive
than MR imaging because, although a
digital mammography unit is much more
expensive than a standard mammogra-
phy unit, it is much less expensive to
purchase and operate than is an MR im-
ager.
The expansion of existing mammo-
graphic core biopsy and preoperative
needle localization techniques to include
enhanced DSM would be straightfor-
ward, given the right equipment. Such
procedures are difficult to perform with
MR imaging guidance because of the ge-
ometry of the MR imager, the time re-
quired for imaging, and the need to work
in a high-strength magnetic field. Dual-
energy enhanced DSM would be espe-
cially well suited for biopsy, since posi-
tioning can be adjusted after injection.
Such adjustment might be needed with a
biopsy device with a small field of view,
because there would be no way to ensure
that a mammographically occult lesion
was included on a precontrast scout im-
age. To allow complete biopsy of an en-
hancing lesion, enhancement would
need to last at least long enough for tar-
geting.
Many aspects of enhanced DSM re-
main to be optimized. Neither the opti-
mal injection rate nor the optimal timing

Volume 229 䡠 Number 1 Digital Subtraction Mammography 䡠 267

 are known, but results in this study indi-
cate acceptable parameters for both. The
two weakly enhancing cancers were im-
aged with nonstandard technique, as a
result of failure of a tubing connection in
Radiology
patient 5 and a slower injection rate in
patient 14 because the intravenous cath-
eter was placed in the hand.
The x-ray energy spectra used in this
study is not optimal for dual-energy io-
dine imaging. The ideal high-energy beam
would have a narrow spectrum centered
just above 33.2 keV. Similarly, the ideal
low-energy beam would be narrow and
centered just below 33.2 keV. The com-
mercial digital mammography unit we
used is designed to produce x-ray ener-
gies that are optimal for unenhanced
mammography. These energies are 18 –23
keV, which is far below the k edge of
iodine, at 33.2 keV. The spectrum output
with either molybdenum or rhodium an-
odes has characteristic peaks in this
range. To have an adequate proportion of
the energy above 33.2 keV for the high-
energy exposure, we use high x-ray beam
voltage and filter the beam with a large
thickness of aluminum. While much of
the low-energy portion of the beam is
filtered, the remaining high-energy por-
tion, as a result of bremsstrahlung, is very
broad and much of it is below 33.2 keV.
268 䡠 Radiology 䡠 October 2003
In the long term, a different anode mate-
rial may be desirable to obtain a more
optimal high-energy beam.
Dual-energy enhanced DSM is capable
of demonstrating cancers that are not vis-
ible at standard mammography. We be-
lieve further studies are warranted for its
evaluation.
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