Ren#{233}

Gilles, MD Jean-Marc
#{149} Guinebreti#{232}re, MD #{149}Lorraine C. Shapeero, MD
Alvian Lesnik, MD Genevieve
#{149} Contesso, MD #{149}Dani#{232}le Sarrazin, MD
Jacques Masselot, MD #{149}Daniel Vanel, MD

Assessment ofBreast Cancer Recurrence

with Contrast-enhanced Subtraction MR
Imaging: Preliminary Results in 26
Patients’

Local relapse
women treated
was suspected
conservatively
in 26
for
T UMORECTOMY combined with radi- gadolinium (0.1 mL/kg
tetraazacyclododecanetetraacetic
of gadolinium-
acid
ation therapy is the standard
breast cancer. All women underwent treatment for small breast cancer (1- [DOTAJ [Andre Guerbet Laboratories,
Aulnay-sous-Bois, France]). These images
routine magnetic resonance (MR) 3). Follow-up of these patients in-
were inspected to select the positions of
imaging and a dynamic MR subtrac- cludes a periodic clinical examination
five sections for dynamic MR study. When
tion study after injection of gadolin- and mammography. Surgery and ra-
no lesions were visible at MR imaging, the
ium-tetraazacyclododecanetetra- diation therapy induce posttherapeu- sections were chosen according to the lo-
acetic acid. Twelve women had no tic sequelae (4-7). Therefore, both cation of the suspect lesion seen on mam-
local relapse. Surgical biopsy en- clinical and mammographic features mograms. The dynamic study was per-
abled confirmation of recurrence in of local recurrences are often nonspe- formed by using a Ti-weighted spin-echo
14 patients. Routine MR imaging did cific (4-8). Ultrasonography (US) is sequence (300/12, 128 x 256 matrix, one
not allow differentiation of recur- sometimes helpful in diagnosing cysts excitation, 47-second acquisition time)
rence from glandular or scar tissue. or fluid collections, but it does not with fat saturation in the sagittal or axial
plane (five images, 3-mm section width,
Except for one case of fat necrosis, allow diagnosis of local relapses
1.5-mm gap, 16-cm field of view). These
patients without local relapse (9,10). Consequently, surgical biopsy
parameters were chosen because previous
showed no contrast enhancement 1 is sometimes the only means of deter-
published results of gadolinium-enhanced
minute 34 seconds after injection. At mining the existence of local relapse. MR imaging have demonstrated contrast
dynamic MR imaging, all recurrences This prospective study was an at- material uptake in malignant breast le-
showed contrast enhancement 1 tempt to determine the value of con- sions I minute 30 seconds after injection
minute 34 seconds after injection. trast material-enhanced subtraction of gadolinium (ii). Because the acquisi-
Nodular enhancement (n = 11) was magnetic resonance (MR) imaging in tion time was 47 seconds, the second im-
found in invasive carcinoma, whereas the assessment of local relapses of age was the most important, being ac-
quired at 1 minute 34 seconds. A set of
linear enhancement was seen in in- breast cancer.
images was acquired before administra-
traductal carcinoma (n = 3). Subtrac-
tion of contrast material. Then, without
tion of precontrast from postcontrast
moving the patient, contrast medium was
images always allowed better visual- MATERIALS AND METHODS injected in less than 10 seconds (bolus
ization of contrast enhancement. technique) and a corresponding set of im-
Between November 1991 and July 1992,
Contrast-enhanced subtraction dy- ages was acquired (total acquisition time, 4
a local relapse was suspected in 26 women
namic MR imaging may prove to be minutes 42 seconds). The precontrast im-
who had been treated for breast cancer at
accurate in diagnosis of local relapses the Institut Gustave Roussy. All of these
ages were then subtracted from the corre-
of breast cancer. sponding postcontrast images on a pixel-
patients had undergone conservative
by-pixel basis with use of the standard
treatment (tumorectomy and external
software subtraction function available on
Index terms: Breast neoplasms, diagnosis, irradiation), and 11 had undergone adju-
our console. Qualitative assessment of
00.31, 00.32 #{149}Breast neoplasms, postoperative, vant treatment: chemotherapy (i = 5),
contrast enhancement was done by one of
00.45, 00.47 #{149}Magnetic resonance (MR), con- castration (ii = 2), or hormonal therapy
the investigators (R.G.). After the dynamic
trast enhancement, 00.12143 Magnetic
#{149} reso- (n = 4).
study, TI-weighted sequences (500/12,
nance (MR), pulse sequences, 00.12149 All patients were prospectively studied
two excitations) with and without fat satu-
with a 1.5-T MR unit (Signa; GE Medical
ration were performed in the sagittal or
Radiology 1993; 188:473-478 Systems, Milwaukee, Wis). Patients lay
axial plane (3-mm section width, 1.5-mm
prone with the breast suspended in a cus-
gap, 16-cm field of view, 256 x 256 ma-
tom-built holder containing a 5-inch (12.7-
trix).
cm)-diameter surface coil. Before exami-
Twenty-two patients underwent surgi-
I From the Departments of Radiology (R.G., nation, an injection site was created,
cal excision within a month after the MR
L.G.S., AL., J.M., DV.), Histology Q.M.G., CC.), usually in a cubital vein, and patients
study. The tumorectomy specimens were
and Radiotherapy (D.S.), Institut Gustave were then placed in the most comfortable
Roussy, 39 Rue Camille Desmoulins, 94805 Ville- sent to the pathologist Q.M.G.), and histo-
position. Ti-weighted images were ac-
juif, France; CIERM, H#{244}pitalBic#{234}tre,Le Krem- logic sections were obtained in the same
quired by using a spin-echo sequence
lin-Bic#{234}tre, France (R.G., AL., J.M., DV.); and plane as in the MR study. Histopathologic
(500/12 [repetition time msec/echo time
Department of Radiology, University of Califor- and MR imaging correlation was per-
msec], two excitations) with and without
nia, San Francisco (L.G.S.). From the 1992 RSNA
fat saturation and T2-weighted images
scientific assembly. Received December 4, 1992;
revision requested January 21, 1993; final revi- (2,500/12-100, two excitations) were ac-
sion received March 16; accepted March 18. Ad- quired in the sagittal or axial plane (3-mm
dress reprint requests to R.G. section width, 1.5-mm gap, 16-cm field of Abbreviation: DOTA = tetraazacyclodo-
e RSNA, 1993 view, 256 x 256 matrix) before injection of decanetetraacetic acid.

473
formed in each case. The following fea-
tures were studied: size and number of Table 1
nodules seen at lumpectomy and mastec- Clinical and Mamniographic Findings in 26 Patients with Suspected Local Relapse
tomy, presence and exact location of fibro- of Breast Cancer
sis and tumor cells inside the nodule, in- Type of Disease
traductal extension within the mastectomy
specimen, and skin and nipple involve- Findings Malignant Benign
ment.
Mammographic findings alone
Microcalcifications 5 1
Abnormal opacity and calcifications 3 1
RESULTS Abnormal opacity 1 4
Patients without Relapse Clinicalfindings alone
Mass 4 5
Local relapse was excluded in 12 Local inflammation 0 1
Mammographic and clinical findings 1 0
patients aged 40-75 years (mean, 57
years). Suspicion of local relapse arose Note-Numbers are numbers of patients.
1-9 years (mean, 5 years) after com-
pletion of treatment and was based
on mammographic (n = 6) or clinical
(n = 6) data (Table 1). In eight pa- Table 2
tients with abnormal opacity or a pal- Patterns of Recurrences and Benign Disease on Routine MR Images
pable mass, US allowed exclusion of a
Before !njectiont
cyst or fluid collection. Surgical bi- Intensity T1WI after
opsy allowed confirmation of absence Pattern* T1WI T2WI Injection
of a relapse in eight patients. In four
Hypointense 3/3 3/2 3/0
cases, since both fine-needle aspira-
Isointense 5/11 5/6 5/10
tion biopsy and MR imaging showed Hyperintense 4/0 4/5 4/4
the suspect lesion to be normal, surgi-
cal biopsy was not performed. In Note-Numbers are number of patients with benign disease/number of patients with malignant dis-
ease.
these cases, no recurrence occurred * The reference tissue was the glandular parenchyma.
during 7-10 months follow-up (mean, t TIWI = TI-weighted images with and without fat saturation, T2WI = 12-weighted images (not ac-
9 months). Histopathologic analysis quired in one patient).

revealed fibrocystic disease without

atypical hyperplasia (n = 1), fibrosis
(n = 2), fat necrosis (n = 4), or fibroad-
enoma (n = 1). MR features on rou- demonstrated invasive carcinoma
Table 3
tine images are listed in Table 2. On (n = 11) and intraductal carcinoma
Results of the Dynamic MR
the MR dynamic subtraction study, with suspected microinvasion (n = 3).
Subtraction Study
no enhancement was observed in Of the 11 invasive carcinomas, four
these benign lesions 1 minute 34 sec- were unifocal, five bifocal (three with Result of Sub traction Study
Final
onds after injection of contrast me- intraductal extension), and two multi- Diagnosis Positive Negative
dium on subtracted images, except in focal. The histopathologic study de-
one case (a patient with fat necrosis) termined the diameter of the 11 recur- Relapse 14 0
(Table 3). In eight of 12 patients, vas- rent invasive carcinomas, which Norelapse 1 11
cular enhancement of subcutaneous ranged from 5 to 70 mm (mean, 14 Note-Numbers are numbers of patients.
vessels was demonstrated on the first mm). MR features on routine images
image of the dynamic MR study, con- are listed in Table 2. On dynamic MR
firming the early vascular phase of subtraction images, all cases of relapse
enhancement. The glandular tissue showed contrast enhancement 1 third, which was outside the field
showed uptake of contrast medium 4 minute 34 seconds after injection of covered by the five sections selected.
minutes 42 seconds (n = 3) or 2 mm- Gd-DOTA, during the early vascular Linear enhancement was seen in all
utes 21 seconds (n = 2) after injection phase (Table 3). At 47 seconds after three cases of intraductal carcinoma
of Gd-DOTA. injection of Gd-DOTA, 13 of 14 pa- (Fig 2). Two nodules measuring 1 mm
tients showed contrast enhancement in diameter in a patient with multifo-
on dynamic MR subtraction images, cal recurrence were overlooked at MR
Patients with Relapse
whereas one patient showed contrast imaging.
In 14 patients aged 40-75 years enhancement only 1 minute 34 sec- In eight of 14 cases, the skin
(mean, 57 years), local recurrence in onds after injection of Gd-DOTA. In showed linear enhancement 1 minute
the breast was confirmed by means of invasive carcinoma, nodular homoge- 34 seconds after injection of contrast
surgical biopsy. Local relapse arose neous (n = 7) or nodular mnhomoge- medium. Histopathologic analysis
3-12 years (mean, 6.4 years) after neous (n = 4) enhancement was seen found sequelae due to radiation ther-
completion of treatment. It was sus- (Fig 1). Inhomogeneous nodular en- apy. In two of these eight cases, nod-
pected on the basis of mammographic hancement always correlated with ular enhancement was associated
(n = 9), clinical (n = 4), or both clinical central fibrosis combined with periph- with linear enhancement of the skin
and mammographic (n = 1) findings eral active tumor at histopathologic on MR images 1 minute 34 seconds
(Table 1). In 10 patients with abnor- analysis. The MR dynamic study re- after injection of gadolinium. Histo-
mal opacity or a palpable mass, US vealed two of three cases of intra- pathologic analysis showed that this
allowed exclusion of a cyst or fluid ductal extension associated with inva- nodular enhancement was due to in-
collection. Histopathologic analysis sive carcinoma but did not show the vasive carcinoma (Fig 3). In 12 pa-

474 Radiology
#{149} August 1993
a. b.

C. d.
Figure 1. MR images of 60-year-old woman treated for intraductal carcinoma of the right breast 12 years earlier. A subcutaneous nodule is
seen in the upper outer quadrant. Mammograms were normal. (a) T2-weighted axial image shows hyperintense scar tissue (arrows), whereas
the round lesion is hypointense (arrowheads). (b, c) Dynamic studies obtained before (b) and 1 minute 34 seconds after (c) injection of contrast
medium show slight enhancement of the round lesion surrounded by fat (arrowheads in c) and of the anterior part of the scar tissue (arrows in
c). (d) Corresponding subtraction image shows obvious enhancement of the round lesion, the nodules of the anterior part of the scar tissue,
and subcutaneous nodules. At histopathologic analysis, all of these nodules proved to be invasive carcinoma (Fig 1 continues).

tients, vascular enhancement was DISCUSSION erative and postirradiation mammo-

demonstrated on the first image of grams are well known (4-7). Focal
the dynamic MR subtraction study, Three prospective, randomized, thickening and retraction at the surgi-
confirming the early vascular phase of controlled trials have shown no dif- cal site, mainly due to surgery, are
enhancement. The glandular tissue ference in overall and disease-free associated with edema and calcifica-
showed uptake of contrast medium 4 survival for tumorectomy and radia- tions due to radiation (4-7). These
minutes 42 seconds (n = 5) or 2 mm- tion therapy versus mastectomy (1-3). features are more pronounced during
utes 21 seconds (n = 2) after injection Conservative therapy has therefore the 1st year after treatment and di-
of gadolinium, masking the recur- become the standard treatment in our minish during the following 2 years.
rences demonstrated 1 minute 34 institution for breast cancer less than Several studies have demonstrated
seconds after injection. In all cases, 3 cm in diameter. Follow-up of pa- a lack of specificity of mammographic
subtraction of early precontrast from tients after conservative treatment features of local recurrences (14-17).
postcontrast images permitted better includes a periodic physical examina- Comparison of follow-up mammo-
visualization of contrast enhance- tion and mammography every 6 grams with a baseline mammogram
ment on dynamic MR studies ac- months during the first 2 years and obtained 6 months after the comple-
quired with fat saturation, because every year thereafter. Local recur- tion of treatment is helpful. Mammog-
only enhancing structures were visu- rences occur at a rate of 1 % per year raphy and US allow good detection of
alized. even long after completion of conser- tumor recurrences, but US results do
Inadequate imaging with the fat vative treatment (12). Early detection not usually alter the management
saturation technique occurred in six of local relapses is known to improve plan in terms of biopsy or follow-up
of the 26 cases in our study, resulting long-term survival after mastectomy determined on the basis of physical
in absence of fat saturation. (12,13). The findings seen on postop- and/or mammographic findings

Volume 188 Number

#{149} 2 Radiolov47S
e. f.
Figure 1 (continued). (e, f) Last images from the dynamic study-with-
out (e) and with (f) subtraction-show enhancement of the scar tissue,
which is masking the nodules. (g) Ti-weighted image with fat satura-
tion obtained after injection of Gd-DOTA shows enhancement masking
the recurrences within the scar.

were found on the MR dynamic

study, except for one intraductal ex-
tension outside the field of explora-
tion of the dynamic study and two
nodules less than 1 mm in diameter
(Fig 1). One of the well-recognized
shortcomings of MR imaging is its
inability to allow detection of micro-
calcifications (21-27). Surprisingly,
when microcalcifications were the
g. only mammographic sign, contrast
enhancement was always seen at dy-
namic MR imaging in our study. His-
(9,10). Among the shortcomings of (11). To date, only one study has eval- topathologic results confirmed that
fine-needle aspiration biopsy are its uated the usefulness of MR imaging these areas of contrast enhancement
poor sensitivity and insufficient sam- in assessing local recurrences of breast were due to invasive carcinoma and
pling rate (18). A negative result cancers, to our knowledge (24). In intraductal carcinoma with suspected
should be interpreted cautiously and that study, T2-weighted images al- microinvasion (Fig 3). One case of fat
should not preclude further investiga- lowed differentiation of scars from necrosis showed enhancement 1
tion of a suspect or equivocal lesion recurrent tumor, but none of the pa- minute 34 seconds after injection of
(18,19). Recently, core needle biopsy tients had an isolated cluster of micro- contrast medium. In this case, the
has demonstrated high accuracy, and calcifications and only 50% of the combination of induration and local
it should be an alternative for obtain- population underwent surgical bi- inflammation warranted surgical bi-
ing a histologic diagnosis nonsurgi- opsy. opsy. The histologic diagnosis was fat
cally (20). However, to date, surgical In our study, routine nondynamic necrosis with surrounding inflamma-
biopsy is frequently the only defini- MR imaging with or without injection tory cells. Contrast enhancement of
tive method of establishing the diag- of Gd-DOTA did not contribute to the subcutaneous vessels helps in assess-
nosis of malignancy. differential diagnosis of recurrence ment of the early vascular phase.
The first studies of MR imaging of versus benign disease (Table 2). On Recent studies have shown the use-
breast disease were disappointing MR dynamic studies, however, all fulness of the fat suppression tech-
(21,22). Recently, many authors have cases of relapse enhanced 1 minute 34 nique in demonstrating contrast en-
emphasized the value of contrast-en- seconds after injection of contrast me- hancement in breast disease (26,27).
hanced MR imaging with a surface dium (Table 3). Morever, correlation In our study, both routine sequences
coil in the diagnosis of breast tumors between histopathologic and MR im- (Ti-weighted sequences) and dy-
(11,23). Malignant lesions exhibit aging results was excellent. Nodular namic sequences were performed
strong, homogeneous enhancement 1 enhancement corresponded to inva- with fat suppression. In addition, mi-
minute 30 seconds after injection, sive carcinoma, whereas linear en- tial precontrast images were sub-
whereas benign lesions show a slower hancement corresponded to intra- tracted from correlative postcontrast
but progressive increase in signal in- ductal carcinoma. Central fibrosis images. In all cases, the subtraction
tensity (11,23). Postlumpectomy scars combined with peripheral tumor cells images allowed better visualization of
show no increase in signal intensity correlated with inhomogeneous en- enhancement than did fat-suppressed
after injection of contrast medium hancement. All multifocal lesions images during dynamic MR study. In

476 Radiology
#{149} August 1993
a. b. C.

d. e. f.
Figure 2. Images of 49-year-old woman treated for invasive carcinoma of the right breast 3 years earlier. (a) Follow-up mammogram
reveals
an isolated cluster of microcalcifications (arrows). (b-e) MR images acquired in the sagittal plane. (b) Ti-weighted image without
fat saturation
obtained before injection of Gd-DOTA shows normal glandular tissue. (c, d) Dynamic studies obtained before (c) and 1 minute 34 seconds af-
ter (d) injection of contrast medium show starlike enhancement (black arrows in d) and subcutaneous vessel (white arrow in d). (e) Corresponding
subtraction image allows better visualization of starlike enhancement (arrows) and the subcutaneous vessel (arrowhead). (f) Histopathologic
slide shows intraductal carcinoma with suspected microinvasion (arrows) (hematoxylin-eosin-safranin stain; original magnification, x 65).

addition, the fat suppression tech- 2. Sarrazin D, L#{233}

M, Rou#{235}sseJ, et al. Conserva- 9. Balu-Maestro C, Bruneton JN, Geoufray A, et
five treatment versus mastectomy in breast al. Ultrasonography post-treatment fol-
nique reduces the number of sections cancer tumors with macroscopic diameter of low-up of breast cancer patients. J Ultrasound
available, and images may prove to be 20 millimeters or less: the experience of the Med 1991; 10:1-7.
Institut Gustave Roussy. Cancer 1984; 53:1209- 10. Mendelson EB. Evaluation of the post-opera-
inadequate (27). Artifacts due to move- 1213. tive breast. Radiol Clin North Am 1992;
ment, respiration, or vascular structures 3. Fischer B, Bauer M, Marolese R, et al. Five- 30:107-138.
year results of a randomized clinical trial corn- 11. Kaiser W, Zeitler E. MR imagin of the
did not inhibit visualization of patho- paring total mastectomy and segmental rnas- breast: fast imaging sequences with and with-
logic enhancement on subtraction im- tectorny with or without radiation in the out Gd-DTPA. Radiology 1989; 170:681-686.
treatment of breast cancer. N EngI J Med 1985; 12. Kurtz JM, Amairic R, Brandone H, et al. Local
ages. Therefore, subtraction images 312:665-673. recurrence after breast-conserving surgery and
should be preferred to fat saturation 4. Sickles E, Herzog K. Mammography of the radiotherapy: frequency, time course, and
postsurgical breast. AIR 1981; 136:585-588. prognosis. Cancer 1989; 63:1912-1917.
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ment of the breast at MR imaging. U cancer: mammography in patient selection Spitalier JM. Results of wide excision for
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Acknowledgments: We thank Lorna Saint- graphic findings after breast cancer treatment 14. Stomper P. Recht A, Berenberg A, Jochelson M,
with local excision and definitive irradiation. Harris J. Mammographic detection of recur-
Ange for editing the manuscript, Corinne
Radiology 1987; 164:455-461. rent cancer in the irradiated breast. AIR 1987;
Brandy for editorial assistance, and Arnaud 7. Sardi A, Eckholdt C, Mckinnon W, Bolton J. 148:39-43.
Ch#{233}ronfor assistance with photography. The significance of marnrnographic findings 15. Dershaw D, McCormick B, Cox L, Osborne M.
after breast-conserving therapy for carcinoma Differentiation of benign and malignant local
of the breast. Surg Gynecol Obstet 1991; 173: tumor recurrence after lumpectomy. AIR 1990;
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Volume 188 Number

#{149} 2 Radiology 477
#{149}
a. b. C.

d. e. f.
Figure 3. Images of 55-year-old woman treated for invasive carcinoma of the right breast 6 years earlier. (a) Follow-up mammogram shows
irregular opacity with cutaneous retraction of the lower quadrants and increased opacity of the upper quadrants. (b) Ti-weighted MR image
without fat saturation shows hypointense scar tissue (arrowheads). (c, d) Dynamic MR images obtained before (c) and i minute 34 seconds af-
ter (d) injection of contrast medium show enhancement of several nodules in the breast and subcutaneous nodule (arrows in d) and subcutane-
ous vessels (white arrowheads in d) and no enhancement of the scar tissue (black arrowheads in d). (e) Corresponding subtraction MR image
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478 Radiology
#{149} August 1993