Nonsurgical Management of High- Risk Lesions Diagnosed at Core Needle Biopsy: Can Malignancy Be Ruled Out Safely With Breast MRI?
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
Wo m e n ’s I m a g i n g • O r i g i n a l R e s e a r c h
Linda et al.
MRI of High-Risk Breast Lesions
Women’s Imaging
Original Research
Nonsurgical Management of High-
Risk Lesions Diagnosed at Core
FOCUS ON:
Downloaded from www.ajronline.org by 213.4.31.4 on 01/26/21 from IP address 213.4.31.4. Copyright ARRS. For personal use only; all rights reserved
Needle Biopsy: Can Malignancy Be
JOURNA L CLUB Ruled Out Safely With Breast MRI?
Anna Linda1 OBJECTIVE. The purpose of this study was to investigate whether breast MRI can be
Chiara Zuiani1 used to rule out malignancy in patients with high-risk lesions diagnosed at imaging-guided
Alessandro Furlan2 core needle biopsy.
Michele Lorenzon1 SUBJECTS AND METHODS. The subjects were women consecutively registered be-
Viviana Londero1 tween October 2004 and April 2010 who had high-risk lesions diagnosed at mammographi-
cally or sonographically guided core needle biopsy and subsequently underwent MRI and
Rossano Girometti1
surgical excision. MR images were reviewed by two experienced breast radiologists. Lesions
Massimo Bazzocchi1 assessed as BI-RADS category 1–3 were considered negative for malignancy, and BI-RADS
Linda A, Zuiani C, Furlan et al. 4 and 5 lesions were considered malignant. Histologic findings at surgical excision were the
reference standard. The sensitivity, specificity, and positive and negative predictive values of
MRI in the detection of associated malignancy were calculated for the entire set of lesions
and for each histologic subtype.
RESULTS. The final sample consisted of 169 high-risk lesions in 166 patients. At
MRI analysis, 116 (68.6%) lesions were considered negative for malignancy, and the other
53 (31.4%) malignant. At surgical excision, 22 malignant lesions were found. The overall
sensitivity, specificity, and positive and negative predictive values of MRI were 72.7% (16/22),
74.8% (110/147), 30.2% (16/53), and 94.8% (110/116). The negative predictive values for
papilloma, radial scar, lobular neoplasia, and atypical ductal hyperplasia were 97.4% (38/39),
97.6% (41/42), 88.0% (22/25), and 90.0% (9/10).
CONCLUSION. Patients with high-risk lesions associated with the lowest likelihood
of malignancy (papilloma and radial scar) and without suspicious MRI findings can safely
undergo follow-up instead of surgery. Because of the low negative predictive value, however,
MRI is not helpful in cases of lobular neoplasia and atypical ductal hyperplasia, and all these
lesions should be excised.
T
he pathologic diagnosis high- gated, but published data are contradictory
risk lesion accounts for as many and nonconclusive [10–18]. In two studies
Keywords: borderline lesions, breast MRI, core needle
biopsy, high-risk lesions, underestimation
as 9% of all imaging-guided core [19, 20], breast MRI was evaluated for pre-
needle biopsies (CNBs) [1–6]. operative detection of malignancy associated
DOI:10.2214/AJR.11.7040 These lesions include lobular neoplasia (LN) with high-risk lesions, and the results were
(lobular carcinoma in situ, atypical lobular promising. The studies, however, were lim-
Received April 15, 2011; accepted after revision
hyperplasia), atypical ductal hyperplasia ited by retrospective design [19] and a rela-
July 22, 2011.
(ADH), papilloma, and radial scar. Because tively small sample size, which did not allow
1
Institute of Diagnostic Radiology, Azienda Ospedaliero– the reported risk of associated malignancy at analysis by lesion [19, 20]. We undertook a
Universitaria Santa Maria della Misericordia, P.le S. surgical excision seems to vary widely (0– large prospective study to investigate wheth-
Maria della Misericordia, 33100 Udine, Italy. Address 35%) [2–7], these lesions are usually man- er breast MRI can be used to safely rule out
correspondence to A. Linda (annalinda33@gmail.com).
aged surgically. However, surgical excision malignancy in patients with high-risk lesions
2
Department of Radiology, University of Pittsburgh, implies increased cost, patient anxiety [8], diagnosed at imaging-guided CNB.
Pittsburgh, PA. and morphologic alteration (i.e., scarring) of
the breast that can hamper interpretation of Subjects and Methods
AJR 2012; 198:272–280
later images [9]. The institutional review board approved this study,
0361–803X/12/1982–272 The role of conventional imaging (mam- which was performed at a large university refer-
mography and sonography) in the manage- ral hospital for breast diseases. All patients provided
© American Roentgen Ray Society ment of high-risk lesions has been investi- written informed consent to participate in the study.
272 AJR:198, February 2012MRI of High-Risk Breast Lesions
Study Sample ages were obtained with a T1-weighted 3D FLASH [21]. In keeping with the BI-RADS lexicon, an
This prospective study was performed between pulse sequence with the following parameters: TR/ assessment of BI-RADS category 1 was used to
October 2004 and April 2010. Included were wom- TE, 15/4.7; flip angle, 25°; matrix size, 197 × 448; indicate absence of contrast enhancement in the
en 18 years old and older with a diagnosis of high- FOV, 350 × 175 mm; section thickness, 1.8 mm; area of the lesion; BI-RADS 2, a benign finding;
risk lesion (LN, ADH, papilloma, radial scar) at acquisition time, 1:28 minutes. From June 2009 BI-RADS 3, a probably benign finding; BI-RADS
imaging-guided CNB who subsequently underwent through April 2010, axial dynamic contrast-en- 4, a suspicious finding; and BI-RADS 5, a finding
breast MRI and surgical excision of the lesion. The hanced images were obtained with a T1-weight- highly suggestive of malignancy. Because of the
Downloaded from www.ajronline.org by 213.4.31.4 on 01/26/21 from IP address 213.4.31.4. Copyright ARRS. For personal use only; all rights reserved
exclusion criteria were presence of synchronous or ed 3D FLASH pulse sequence with the following selection criteria, BI-RADS category 6 (known
metachronous carcinoma (ductal carcinoma in situ parameters: TR/TE, 9/4.7; flip angle, 25°; matrix cancer) was not considered an option.
[DCIS], invasive carcinoma) in the same breast; size, 512 × 512; FOV, 340 × 340 mm; section
contraindications to MRI (pacemaker, claustropho- thickness, 2 mm; acquisition time, 1:20 minutes. Reference Standard
bia, vascular clip); severe limitation to MR image Gadobenate dimeglumine (MultiHance, Bracco) The reference standard was the result at histo-
interpretation (e.g., movement artifacts); lack of fi- was administered IV by automated bolus injection pathologic examination of the surgically excised
nal pathologic result after surgical excision because at a dose of 0.1 mmol/kg body weight with a flow specimen. Invasive cancer and DCIS were classi-
patient declined surgical treatment or was referred rate of 2 mL/s immediately followed by flushing of fied as malignant, and all other pathologic find-
to an outside hospital; and surgical excision per- 20 mL of saline solution with an automatic injector ings as benign. Histopathologic examinations
formed more than 3 months after CNB. Patient en- (Spectris Solaris, MedRad). Images were acquired were performed by a breast pathologist with more
rollment and consent took place at the time of diag- sequentially once before and five times after injec- than 10 years of experience.
nosis of a high-risk lesion. tion of the contrast agent, beginning 12 seconds af-
ter initiation of the contrast injection and with no Statistical Analysis
Percutaneous Core Needle Biopsy delay between images. Rates of underestimation of malignancy (num-
Percutaneous CNB was performed under Postprocessing and construction of dynam- ber of high-risk lesions upgraded to malignancy at
mammographic or sonographic guidance accord- ic curves were performed at a workstation (Syn- surgical excision divided by the number of high-
ing to the judgment of the attending radiologist. go MultiModality Workplace, Leonardo, Siemens risk lesions surgically excised) were calculated
The biopsy procedures were performed by radiol- Healthcare) by one of five radiologists (more than overall, for each high-risk lesion type (radial scar,
ogists with 10–20 years’ experience in breast im- 2 years of experience in breast MRI). Postpro- papilloma, LN, ADH), and for biopsy type (so-
aging. In cases of sonographically guided CNB, cessing included temporal subtraction (all con- nographically guided CNB, mammographically
an automated biopsy gun (Magnum Biopsy In- trast-enhanced images minus unenhanced imag- guided vacuum-assisted biopsy).
strument, Bard) or a semiautomated biopsy gun es) and generation of multiplanar reconstruction For the purposes of computing the diagnostic
(Precisa, HS Hospital Service) with a 14-gauge, and maximum intensity projections. Dynamic sig- yield of MRI, results of image evaluation were
15-cm-long needle (throw of needle, 23 mm) was nal intensity–time curves were constructed for re- dichotomized as negative for malignancy (BI-
used. A mean of five core samples (range, three gions of interest (3 × 3 pixels) positioned with- RADS categories 1–3) and positive for malig-
to eight) were obtained per lesion. In cases of in the lesion on subjectively determined areas of nancy (BI-RADS categories 4 and 5). Malignant
small lesions, an amagnetic, sonographically vis- maximal enhancement. lesions assessed as positive on MR images were
ible clip (GelMark, UltraCor) was left in place to considered true-positive cases and those assessed
mark the biopsy site. In cases in which a mam- MRI Analysis as negative were considered false-negative cases.
mographically detected lesion was not identified The study coordinator (more than 5 years of ex- Benign lesions assessed as positive on MR imag-
at sonographic examination, CNB was performed perience in breast imaging), who was not involved in es were considered false-positive cases, and those
under mammographic guidance on a digital prone further MRI evaluation, reviewed all images avail- assessed as negative were considered true-nega-
table (Mammobed Giotto, IMS) with a direction- able and annotated on a breast map the location of tive cases. On the basis of these data, the sensitiv-
al vacuum-assisted biopsy device (Mammotome, each biopsied lesion using clock-face referents and ity, specificity, and positive and negative predic-
Mammotome) with an 11-gauge needle. On aver- relative distance from the nipple. The maps were dis- tive values of MRI in the detection of malignancy
age, 12 core samples (range, nine to 18) were ob- tributed to the readers before image interpretation. were calculated. Exact 95% CI was computed for
tained per lesion. In patients with mammograph- At acquisition, two independent radiologists each performance measure. The performance pa-
ically detected microcalcifications, a specimen with more than 10 years of experience in breast rameters were specifically calculated for each
radiograph was obtained to confirm the presence imaging, including breast MRI, prospective- high-risk lesion and for biopsy type. The Pearson
of calcifications in each sample, and a clip (Mam- ly evaluated the images at the workstation. Any chi-square test was used to compare performance
moMark, Mammotome) was left in place to mark discrepancy in opinion was resolved by consen- parameters among groups. A value of p < 0.05
the biopsy site. sus. The readers were aware of the lesion location was considered indicative of a statistically sig-
and of the histologic diagnosis at CNB. So that in- nificant difference. All statistical analyses were
MRI Technique formation on the performance of MRI would be performed with commercially available software
Breast MRI studies were performed with a 1.5- obtained independently of mammographic and (MedCalc 9.2.0.1, MedCalc Software).
T system (Magnetom Avanto, Siemens Health- sonographic features, mammographic and sono-
care) with a dedicated bilateral surface breast coil graphic images were not available to the readers Results
and the patient prone. For premenopausal patients, at MR image interpretation. Unenhanced and con- Patients and Lesions
MRI was performed during the second week of trast-enhanced MR images were evaluated. Mor- A total of 3243 imaging-guided CNBs of
the menstrual cycle. From October 2004 through phologic and kinetic evaluation and lesion assess- the breast were performed in our department
May 2009, coronal dynamic contrast-enhanced im- ment were based on the BI-RADS MRI lexicon during the study period. Among them, 2514
AJR:198, February 2012 273Downloaded from www.ajronline.org by 213.4.31.4 on 01/26/21 from IP address 213.4.31.4. Copyright ARRS. For personal use only; all rights reserved
TABLE 1: Imaging Features of 22 Lesions Diagnosed as High-Risk at Core Needle Biopsy With Finding of Malignancy After Surgical Excision
274
Core Needle Biopsy Final Pathologic Finding Conventional Imaging Finding MRI Finding
Mass Nonmasslike Enhancement
Lesion Assessment Size Internal Internal Signal Intensity– BI-RADS
No. of Finding Diagnosis Type Histologic Type, Grade (mm)a Mammography Ultrasound Shape Margin Enhancement Distribution enhancement Time Curve Type Category
1b False-negative Papilloma Ultrasound core needle DCIS, low 4 Occult Nodule Lobulated Irregular Homogeneous — — 2 3
2 True-positive Papilloma Ultrasound core needle DCIS, low NA NA Dilated ducts Irregular Smooth Homogeneous — — 3 4
3 True-positive Papilloma Ultrasound core needle DCIS, high 30 NA Dilated ducts Lobulated Irregular Homogeneous Regional Inhomogeneous 2 4
4 True-positive Papilloma Ultrasound core needle DCIS, intermediate NA Occult Nodule Oval Irregular Inhomogeneous — — 3 4
5 True-positive Radial scar Ultrasound core needle ILC, intermediate 5 Distortion Nodule Irregular Irregular Inhomogeneous — — 2 4
6 False-negative Radial scar Ultrasound core needle DCIS, low 8 Occult Nodule — — — — — — 1
7 True-positive LN Mammographic vacuum ILC, intermediate 4 Microscopic Occult Irregular Irregular Inhomogeneous — — 2 4
assisted
8 False-negative LN Mammographic vacuum DCIS, intermediate 4 Microscopic Occult — — — — — — 1
assisted
9 True-positive LN Mammographic vacuum DCIS, high 2 Microscopic Occult Irregular Irregular Inhomogeneous — — 2 4
assisted
10 True-positive LN Ultrasound core needle Invasive tubulolobular 20 Occult Nodule Lobulated Irregular Inhomogeneous — — 2 4
carcinoma,
intermediate
11 False-negative LN Ultrasound core needle ILC, intermediate 4 Occult Nodule Oval Regular Homogeneous — — 2 3
12 True-positive LN Ultrasound core needle ILC, intermediate 10 Occult Nodule Irregular Irregular Inhomogeneous — — 2 4
Linda et al.
13 True-positive LN Ultrasound core needle ILC, intermediate 11 Occult Nodule Oval Irregular Inhomogeneous — — 2 4
14 False-negative LN Mammographic vacuum DCIS, low 5 Microscopic Occult — — — — — — 1
assisted
15c True-positive LN Mammographic vacuum DCIS, low NA Microscopic Occult — — — Ductal Inhomogeneous 2 4
assisted
16 True-positive LN Ultrasound core needle ILC, intermediate 5 Occult Nodule Oval Irregular Inhomogeneous — — 2 4
17 True-positive LN Ultrasound core needle DCIS, low NA Occult Nodule Irregular Irregular Inhomogeneous — — 2 4
18 True-positive LN Mammographic vacuum DCIS, intermediate NA Microscopic Occult Oval Irregular Inhomogeneous — — 2 4
assisted
19 False-negative ADH Ultrasound core needle DCIS, intermediate NA Occult Hypoechoic — — — — — — 1
area
20 True-positive ADH Mammographic vacuum DCIS, low 5 Microscopic Occult — — — Segmental Inhomogeneous 2 4
assisted
21 True-positive ADH Ultrasound core needle DCIS, low 10 Occult Hypoechoic — — — Focal Inhomogeneous 3 4
area
22 True-positive ADH Mammographic vacuum Invasive ductal- 7 Microscopic Occult Round Irregular Inhomogeneous — — 2 4
assisted lobular carcinoma,
intermediate
Note—Note—Dash (—) indicates not assessable. DCIS = ductal carcinoma in situ, NA = not available, ILC = invasive lobular carcinoma, LN = lobular neoplasia, ADH = atypical ductal hyperplasia.
aNeoplastic component.
bFigure 4.
AJR:198, February 2012
cFigure 1.MRI of High-Risk Breast Lesions
(77.6%) were performed under sonographic TABLE 2: Rate of Underestimation of Malignancy at Biopsy
guidance and 729 (22.4%) under stereotac-
No. of Malignancy Underestimation Rate (%)b
tic guidance. Two hundred forty-one (7.4%) Pathologic Lesions
high-risk lesions were diagnosed consecu- Diagnosis at Biopsy Type of Biopsya By Biopsy Type Overall
tively in 236 women. Three patients (three
Papilloma 64 Ultrasound core needle (60) 6.7 (4/60) 6.2 (4/64)
lesions) were excluded because of the pres-
ence of ipsilateral breast cancer. Four pa- Mammographic vacuum assisted (4) 0 (0/4)
Downloaded from www.ajronline.org by 213.4.31.4 on 01/26/21 from IP address 213.4.31.4. Copyright ARRS. For personal use only; all rights reserved
tients (four lesions) had contraindications to Radial scar 54 Ultrasound core needle (41) 4.9 (2/41) 3.7 (2/54)
MRI. All other patients consented to partici- Mammographic vacuum assisted (13) 0 (0/13)
pation in the study and were enrolled. How-
Lobular neoplasia 35 Ultrasound core needle (15) 40.0 (6/15) 34.3 (12/35)
ever, 63 patients (65 lesions) did not com-
plete the study because they were later found Mammographic vacuum assisted (20) 30.0 (6/20)
to be ineligible owing to the presence of ar- Atypical ductal 16 Ultrasound core needle (6) 33.3 (2/6) 25.0 (4/16)
tifacts limiting MRI interpretation (eight pa- hyperplasia
tients with eight lesions) or because they de- Mammographic vacuum assisted (10) 20.0 (2/10)
clined surgery (55 patients with 57 lesions). Total 169 Ultrasound core needle (122) 11.5 (14/122) 13.0 (22/169)
The final sample included 166 patients
Mammographic vacuum assisted (47) 17.0 (8/47)
(mean age, 52.2 years; range, 25–76 years)
with 169 high-risk lesions. Of these patients, Note—Values in parentheses are numbers of lesions. CNB = core needle biopsy.
aValues in parentheses are numbers of lesions.
164 had one high-risk lesion, one patient had bValues in parentheses are number of lesions upgraded.
two synchronous ipsilateral high-risk lesions,
and one patient had three synchronous high- category 2, and 45 (26.6%) BI-RADS catego- The other six (5.2%) lesions (four BI-RADS
risk lesions, two in one breast and one in the ry 3. The other 53 (31.4%) lesions were con- 1, two BI-RADS 3) were upgraded to malig-
other breast. Of the 169 high-risk lesions, sidered positive: 51 (30.2%) BI-RADS cate- nancy (false-negative) (Fig. 4). The overall
122 (72.2%) were biopsied under sonograph- gory 4 and 2 (1.2%) BI-RADS category 5. Of sensitivity, specificity, and positive and neg-
ic guidance and 47 (27.8%) under mammo- the 53 lesions assessed as positive at MRI, 16 ative predictive values of MRI in the identi-
graphic guidance. At examination of the biop- (30.2%) lesions (all BI-RADS 4) proved ma- fication of malignancy were 72.7% (95% CI,
sy specimen, 64 (37.9%) lesions were found to lignant (true-positive) (Fig. 1) at surgical ex- 65–79%; 16/22), 74.8% (95% CI, 67–81%;
be papilloma without atypia; 54 (31.9%), radi- cision, and 37 (69.8%) lesions (35 BI-RADS 110/147), 30.2% (95% CI, 23–38%; 16/53),
al scar; 35 (20.7%), LN; and 16 (9.5%), ADH. 4, two BI-RADS 5) proved benign (false- and 94.8% (95% CI, 90–97%; 110/116). The
The mean interval between biopsy and MRI positive) (Fig. 2). Of 116 lesions classified performance parameters for lesions diag-
was 11 days (range, 3–25 days). as negative at MRI, 110 (94.8%) lesions (55 nosed at sonographically guided CNB and for
BI-RADS 1, 12 BI-RADS 2, 43 BI-RADS those diagnosed at mammographically guid-
Histologic Results at Surgical Excision 3) were confirmed as benign at final patho- ed vacuum-assisted biopsy are shown in Ta-
Surgical excision was performed 10–75 logic examination (true-negative) (Fig. 3). ble 3. The negative predictive values for papil-
days after biopsy (mean, 23 days) and 6–69
days after MRI (mean, 19 days). Histopatho-
logic examination of the surgical specimens
revealed 22 malignant lesions. Of these, 14
(63.6%) were DCIS (eight low grade, four
intermediate grade, and two high grade),
and the other eight (36.4%) were invasive
carcinoma (six intermediate-grade invasive
lobular carcinoma, one intermediate-grade
invasive ductal-lobular carcinoma, one in-
termediate-grade invasive tubulolobular car-
cinoma) (Table 1). The overall biopsy un-
derestimation rate was 13% (22/169). The
underestimation rates among lesions diag-
nosed under sonographic guidance and le-
sions diagnosed under mammographic guid-
ance were 11.5% (14/122) and 17.0% (8/47) A B
(p = 0.559) (Table 2). Fig. 1—61-year-old woman with low-grade ductal carcinoma in situ and true-positive findings at MRI (lesion 15).
A, Magnification mammogram (retroareolar region of left breast) shows 10-mm cluster of amorphous
MRI Analysis Against Reference Standard calcifications (arrow). Ultrasound findings were normal. Mammographically guided vacuum-assisted biopsy
At breast MRI analysis, 116 (68.6%) le- result was lobular neoplasia.
B, Axial T1-weighted contrast-enhanced subtracted MR image (TR/TE, 9/4.7; flip angle, 25°) shows nonmasslike
sions were assessed as negative: 59 (34.9%) enhancing lesion (arrow) with ductal distribution and inhomogeneous enhancement in retroareolar region of left
BI-RADS category 1, 12 (7.1%) BI-RADS breast. Lesion had type 2 signal intensity curve and was classified BI-RADS category 4.
AJR:198, February 2012 275Linda et al.
Downloaded from www.ajronline.org by 213.4.31.4 on 01/26/21 from IP address 213.4.31.4. Copyright ARRS. For personal use only; all rights reserved
A B C
Fig. 2—48-year-old woman with radial scar and false-positive MRI findings.
A, Left craniocaudal mammogram shows area of focal asymmetric density and architectural distortion (arrow) in outer quadrants of breast.
B, Correlative ultrasound scan shows hypoechoic area (arrow) with irregular shape and margins and posterior acoustic shadowing measuring 20 mm. Sonographically
guided 14-gauge core needle biopsy result was radial scar.
C, Coronal T1-weighted contrast-enhanced subtracted MR image (TR/TE, 15/4; flip angle, 7.25° ) shows masslike enhancing lesion (arrow) with irregular shape and margins
and inhomogeneous enhancement measuring 22 mm in outer quadrants of left breast. Lesion had type 3 signal intensity curve and was classified as BI-RADS category 4.
loma, radial scar, LN, and ADH were 97.4% predictive of upgrade to malignancy. All of pared with LN and ADH (88% and 90%).
(95% CI, 89–100%; 38/39), 97.6% (95% CI, those lesions were enhancing, but we found Presumably, the variability in likelihood of
88–100%; 41/42), 88.0% (95% CI, 72–96%; that approximately one half of benign high- malignancy among high-risk lesions may af-
22/25), and 90.0% (95% CI, 63–99%; 9/10). risk lesions were not enhancing (classified fect the usefulness of MRI in prediction of the
All performance parameters for each high- BI-RADS category 1). On the other hand, presence or absence of malignancy. Papillo-
risk lesion type are reported in Table 4. four of 22 high-risk lesions upgraded to ma- mas and radial scars diagnosed at CNB are
lignancy (one radial scar, two LN, one ADH) associated with much lower prevalence of
Discussion in our series were nonenhancing at MRI. All malignancy at surgical excision than are LN
Our data showed that breast MRI can be these lesions corresponded to small DCIS of and ADH (6.2% and 3.7% versus 34.3% and
used to identify high-risk lesions associated low or intermediate grade (Table 1). It is rea- 25.0% in our study) [2–6]. Because of the low
with a low likelihood of upgrade to malig- sonable to believe that absence of enhance- prevalence of disease, it is not surprising that
nancy at surgical excision. The overall sen- ment may be a strong indicator of absence of MRI had a high negative predictive value in
sitivity is 72.7%; specificity, 74.8%; positive invasive carcinoma. Further studies are nec- these two specific groups [24]. If on the ba-
predictive value, 30.2%; and negative pre- essary to clarify this issue. sis of low risk of malignancy, all papillomas
dictive value, 94.8%. These results suggest High negative predictive values for malig- and radial scars with normal MRI findings in
a possible role for this noninvasive imag- nancy were found for papilloma without atyp- our study had been hypothetically addressed
ing modality in the workup of high-risk le- ia and radial scar (97.4% and 97.6%), com- with follow-up [25], 79 unnecessary surgi-
sions. Despite differences in study methods,
our findings are similar to those reported in TABLE 3: Performance of MRI Based on Type of Biopsy
a retrospective study [19] of 79 lesions eval- Biopsy Type
uated with the Baum-Fisher score [22] and
in another prospective study [20] of 32 le- Mammographic Ultrasound Core
sions. The results of both studies confirmed Parameter Vacuum-Assisted Biopsy Needle Biopsy p
that MRI has high negative predictive value Sensitivity 62.5 (47–76) 78.6 (70–85) 0.985
for malignancy (98.2% and 96%) in the eval- Specificity 94.9 (83–99) 67.6 (58–76) 0.272
uation of high-risk lesions.
Positive predictive value 71.4 (56–83) 23.9 (17–33) 0.196
Strigel et al. [23] evaluated 39 high-risk
lesions initially detected with MRI and Negative predictive value 92.5 (80–98) 96.1 (90–99) 0.995
found no specific morphologic MRI features Note—Biopsy type values are percentages with 95% CI in parentheses.
276 AJR:198, February 2012MRI of High-Risk Breast Lesions
TABLE 4: Overall Performance of MRI
Lesion Type
Parameter Papilloma Radial Scar Lobular Neoplasia Atypical Ductal Hyperplasia Overall
Sensitivity 75.0 (62–85) 50.0 (36–64) 75.0 (57–87) 75.0 (47–92) 72.7 (65–79)
Specificity 63.3 (50–75) 78.8 (65–88) 95.7 (81– 99) 75.0 (47– 92) 74.8 (67–81)
Positive predictive value 12.0 (6–23) 8.3 (3–20) 90.0 (74– 97) 50.0 (25–74) 30.2 (23– 38)
Downloaded from www.ajronline.org by 213.4.31.4 on 01/26/21 from IP address 213.4.31.4. Copyright ARRS. For personal use only; all rights reserved
Negative predictive value 97.4 (89–100) 97.6 (88–100) 88.0 (72–96) 90.0 (63–99) 94.8 (90–97)
Note—Data are percentages with 95% CI in parentheses.
cal procedures would have been avoided, and 27]. On the other hand, low-grade DCIS has a We propose that women with papilloma
two false-negative cases (one in each group) benign biologic profile and if left undetected without atypia and those with radial scar
would have been missed. Both these false- (and untreated), it is likely to remain dormant with normal MRI findings may safely un-
negative lesions were found to be low-grade or to exhibit slow (decades long) progression dergo clinical and radiologic follow-up. A
DCIS (4 and 8 mm) at pathologic examina- to invasive carcinoma [28]. Therefore, diag- possible interval time for follow-up might be
tion of the surgical specimen (lesions 1 and nostic delay due to noninvasive management every 6 months for 2 years with both con-
6, Table 1). It has been reported that absence (imaging follow-up) in our two false-negative ventional imaging and MRI for prompt rec-
of enhancement on MR images is observed cases would probably not have a substantial ognition of interval onset of contrast en-
in 20–60% of cases of low-grade DCIS [26, effect on prognosis. hancement [20]. MRI had an unacceptably
A B C
Fig. 3—47-year-old woman with sclerosing papilloma and true-negative MRI findings.
A, Mediolateral oblique mammogram shows low-density oval opacity (arrow) with regular margins in upper retroareolar area of right breast.
B, Ultrasound scan corresponding to A shows oval hypoechoic nodule with regular margins (calipers) measuring 8 mm. Sonographically guided 14-gauge core needle
biopsy result was sclerosing papilloma without atypia.
C, Axial T1-weighted contrast-enhanced subtracted MR image (TR/TE, 9/4.7; flip angle, 25°) shows oval mass (arrow) with smooth margins and homogeneous
enhancement in upper retroareolar area of right breast. Lesion had type 2 signal intensity curve and was classified BI-RADS category 3.
Fig. 4—62-year-old woman with low-
grade ductal carcinoma in situ (4 mm) and
false-negative findings at MRI (lesion 1).
A, Ultrasound scan of left breast shows
hypoechoic nodule (arrow) with lobulated
shape and slightly irregular margins
measuring 11 mm in upper outer quadrant
of breast. Mammographic findings were
normal. Sonographically guided 14-gauge
core needle biopsy result was papilloma
without atypia.
B, Axial T1-weighted contrast-enhanced
subtracted MR image (TR/TE, 9/4; flip
angle, 7.25°) shows lobulated mass (arrow)
with predominantly regular margins and
homogeneous enhancement in upper outer
quadrant of left breast. Lesion had type 2
signal intensity curve and was classified
A B BI-RADS 3.
AJR:198, February 2012 277Linda et al.
low negative predictive value for malignan- LN seem not to benefit from MRI, and these 11. Nagi CS, O’Donnell JE, Tismenetsky M, Blei-
cy in patients with LN and ADH (88% and lesions should be surgically excised. weiss IJ, Jaffer SM. Lobular neoplasia on core
90%), corresponding to 12% and 10% false- needle biopsy does not require excision. Cancer
negative rates. According to our data, MRI Acknowledgment 2008; 112:2152–2158
cannot be recommended in the management We thank Luisa Battigelli, University of 12. Lam WW, Chu WC, Tang AP, Tse G, Ma TK.
decision process for LN and ADH. These le- Udine, Italy, for data collection and image Role of radiologic features in the management of
sions should be excised because of the high preparation. papillary lesions of the breast. AJR 2006; 186:
Downloaded from www.ajronline.org by 213.4.31.4 on 01/26/21 from IP address 213.4.31.4. Copyright ARRS. For personal use only; all rights reserved
upgrade rate. Further studies are needed to 1322–1327
establish the most appropriate time inter- References 13. Shin HJ, Kim HH, Kim SM, et al. Papillary le-
vals and modalities for imaging follow-up, 1. Schueller G, Jaromi S, Ponhold L, et al. US-guid- sions of the breast diagnosed at percutaneous so-
to assess cost-effectiveness, and to gauge pa- ed 14-gauge core-needle breast biopsy: results of a nographically guided biopsy: comparison of so-
tients’ perceptions of this approach. validation study in 1352 cases. Radiology 2008; nographic features and biopsy methods. AJR
Our study had limitations. First was the 248:406–413 2008; 190:630–636
small number of ADH lesions—correspond- 2. Lee AH, Denley HE, Pinder SE, et al. Excision 14. Youk JH, Kim EK, Kwak JY, Son EJ, Park BW,
ing to 9.5% of all high-risk lesions—com- biopsy findings of patients with breast needle core Kim SI. Benign papilloma without atypia diag-
pared with the number in most other studies biopsies reported as suspicious of malignancy nosed at US-guided 14-gauge core-needle biopsy:
[2, 4–6, 20]. Selection bias can be excluded (B4) or lesion of uncertain malignant potential clinical and US features predictive of upgrade to
on the basis of the study design (consecutive (B3). Histopathology 2003; 42:331–336 malignancy. Radiology 2011; 258:81–88
prospective recruitment). Instead, the under- 3. Londero V, Zuiani C, Linda A, Battigelli L, Bron- 15. Linda A, Zuiani C, Furlan A, et al. Radial scars
representation of ADH, which usually pres- dani G, Bazzocchi M. Borderline breast lesions: without atypia diagnosed at imaging-guided nee-
ents as microcalcifications [29, 30], may be comparison of malignancy underestimation rates dle biopsy: how often is associated malignancy
attributed to the small number of biopsies with 14-gauge core needle biopsy versus 11-gauge found at subsequent surgical excision, and do
performed under mammographic guidance in vacuum-assisted device. Eur Radiol 2011; 21: mammography and sonography predict which le-
our series (47/169). In addition, the pathologic 1200–1206 sions are malignant? AJR 2010; 194:1146–1151
differential diagnosis of ADH and low-grade 4. Rakha EA, Lee AH, Jenkins JA, Murphy AE, 16. Brenner RJ, Jackman RJ, Parker SH, et al. Percu-
DCIS is known to be challenging and to have Hamilton LJ, Ellis IO. Characterization and out- taneous core needle biopsy of radial scars of the
substantial interobserver variability, even come of breast needle core biopsy diagnoses of breast: when is excision necessary? AJR 2002;
when strict criteria are used [31, 32]. This lesions of uncertain malignant potential (B3) in 179:1179–1184
finding further emphasizes the importance of abnormalities detected by mammographic 17. Youk JH, Kim EK, Kim MJ. Atypical ductal hy-
by-lesion analysis to ensure reproducibility of screening. Int J Cancer 2010; 129:1417–1424 perplasia diagnosed at sonographically guided
the results for differing spectra of high-risk 5. El-Sayed ME, Rakha EA, Reed J, Lee AH, Evans 14-gauge core needle biopsy of breast mass. AJR
lesions. The second limitation was the small AJ, Ellis IO. Predictive value of needle core bi- 2009; 192:1135–1141
proportion of lesions diagnosed at mammo- opsy diagnoses of lesions of uncertain malignant 18. Hoang JK, Hill P, Cawson JN. Can mammograph-
graphically guided biopsy (21.9%). However, potential (B3) in abnormalities detected by mam- ic findings help discriminate between atypical
our results are in agreement with those of a mographic screening. Histopathology 2008; ductal hyperplasia and ductal carcinoma in situ
previous study [20] of 32 high-risk lesions all 53:650–657 after needle core biopsy? Breast 2008; 17:282–288
diagnosed at sonographically guided CNB. 6. Houssami N, Ciatto S, Bilous M, Vezzosi V, Bian- 19. Linda A, Zuiani C, Bazzocchi M, Furlan A, Londero
In addition, we found no statistically signifi- chi S. Borderline breast core needle histology: V. Borderline breast lesions diagnosed at core needle
cant differences between mammographically predictive values for malignancy in lesions of un- biopsy: can magnetic resonance mammography rule
guided vacuum-assisted biopsy and sonogra- certain malignant potential (B3). Br J Cancer out associated malignancy? Preliminary results based
phically guided CNB with respect to the per- 2007; 96:1253–1257 on 79 surgically excised lesions. Breast 2008; 17:
formance of MRI in the diagnosis of lesions. 7. Georgian-Smith D, Lawton TJ. Controversies on 125–131
Third, analysis of interobserver variability in the management of high-risk lesions at core biop- 20. Pediconi F, Padula S, Dominelli V, et al. Role of
MRI interpretation in this clinical situation sy from a radiology/pathology perspective. Radi- breast MR imaging for predicting malignancy of
was not performed. Fourth, the acquisition ol Clin North Am 2010; 48:999–1012 histologically borderline lesions diagnosed at core
plane of MR images was coronal in the ini- 8. Golub RM, Bennett CL, Stinson T, Venta L, Mor- needle biopsy: prospective evaluation. Radiology
tial phase of the study period and in the axial row M. Cost minimization study of image-guided 2010; 257:653–661
plane later. However, both imaging planes are core biopsy versus surgical excisional biopsy for 21. Ikeda DM, Hylton NM, Kuhl CK, et al. BI-RADS:
currently considered appropriate for bilateral women with abnormal mammograms. J Clin On- magnetic resonance imaging, 1st ed. In: D’Orsi
dynamic MRI [33]. col 2004; 22:2430–2437 CJ, Mendelson EB, Ikeda DM, et al. Breast Imag-
9. March DE, Raslavicus A, Coughlin BF, Klein SV, ing Reporting and Data System: ACR BI-RADS—
Conclusion Makari-Judson G. Use of breast core biopsy in the breast imaging atlas. Reston, VA: American Col-
Our results suggest that patients with high- United States: results of a national survey. AJR lege of Radiology, 2003
risk lesions associated with the lowest likeli- 1997; 169:697–701 22. Baum F, Fischer U, Vosshenrich R, Grabbe E.
hood of malignancy (papilloma without atyp- 10. Brem RF, Lechner MC, Jackman RJ, et al. Lobu- Classification of hypervascularized lesions in CE
ia and radial scar) and without suspicious MRI lar neoplasia at percutaneous breast biopsy: vari- MR imaging of the breast. Eur Radiol 2002;
findings can safely undergo follow-up instead ables associated with carcinoma at surgical exci- 12:1087–1092
of surgical excision. Patients with ADH and sion. AJR 2008; 190:637–641 23. Strigel RM, Eby PR, Demartini WB, et al. Fre-
278 AJR:198, February 2012MRI of High-Risk Breast Lesions
quency, upgrade rates, and characteristics of high- morphological pattern of enhancement. Br J Ra- frequency and mammographic and pathologic re-
risk lesions initially identified with breast MRI. diol 2003; 76:3–12 lationships in excisional biopsies guided with
AJR 2010; 195:792–798 27. Kuhl CK, Schrading S, Bieling HB, et al. MRI for mammography and clinical examination. Radiol-
24. Langlotz CP. Fundamental measures of diagnos- diagnosis of pure ductal carcinoma in situ: a pro- ogy 1993; 189:667–671
tic examination performance: usefulness for clini- spective observational study. Lancet 2007; 31. Eby PR, Ochsner JE, DeMartini WB, Allison
cal decision making and research. Radiology 370:485–492 KH, Peacock S, Lehman CD. Is surgical excision
2003; 228:3–9 28. Sanders ME, Schuyler PA, Dupont WD, Page D. necessary for focal atypical ductal hyperplasia
Downloaded from www.ajronline.org by 213.4.31.4 on 01/26/21 from IP address 213.4.31.4. Copyright ARRS. For personal use only; all rights reserved
25. Jackman RJ, Nowels KW, Rodriguez-Soto J, Mar- The natural history of low-grade ductal carcino- found at stereotactic vacuum-assisted breast bi-
zoni FA Jr, Finkelstein SI, Shepard MJ. Stereotac- ma in situ of the breast in women treated by biop- opsy? Ann Surg Oncol 2008; 15:3232–3238
tic, automated, large-core needle biopsy of non- sy only revealed over 30 years of long-term fol- 32. Schnitt SJ, Connolly JL, Tavassoli FA, et al. In-
palpable breast lesions: false-negative and low-up. Cancer 2005; 103:2481–2484 terobserver reproducibility in the diagnosis of duc-
histologic underestimation rates after long-term 29. Helvie MA, Hessler C, Frank TS, Ikeda DM. tal proliferative breast lesions using standardized
follow-up. Radiology 1999; 210:799–805 Atypical hyperplasia of the breast: mammograph- criteria. Am J Surg Pathol 1992; 16:1133–1143
26. Neubauer H, Li M, Kuehne-Heid R, Schneider A, ic appearance and histologic correlation. Radiolo- 33. Kuhl C. The current status of breast MR imaging.
Kaiser WA. High grade and non-high grade ductal gy 1991; 179:759–764 Part I. Choice of technique, image interpretation,
carcinoma in situ on dynamic MR mammogra- 30. Stomper PC, Cholewinski SP, Penetrante RB, diagnostic accuracy, and transfer to clinical prac-
phy: characteristic findings for signal increase and Harlos JP, Tsangaris TN. Atypical hyperplasia: tice. Radiology 2007; 244:356–378
F O R YO U R I N F O R M AT I O N
This article has been selected for the new AJR Journal Club activity. The accompanying Journal
Club study guide can be found on the following page.
AJR:198, February 2012 279Linda et al.
A PP E N D I X 1 : A J R J o u r n a l C l u b
Study Guide:
Nonsurgical Management of High-Risk Lesions Diagnosed at Core
Needle Biopsy: Can Malignancy Be Ruled Out Safely With Breast MRI?
Downloaded from www.ajronline.org by 213.4.31.4 on 01/26/21 from IP address 213.4.31.4. Copyright ARRS. For personal use only; all rights reserved
Joseph J. Budovec, Margaret Mulligan, Alan Mautz
Medical College of Wisconsin, Milwaukee, WI
jbudovec@mcw.edu, mmulliga@mcw.edu, amautz@mcw.edu
Introduction
1. Is the research question clinically relevant? Is the topic timely?
2. What is the standard practice at your institution for management of high-risk lesions diagnosed at core needle biopsy?
3. What is the research question being asked? Is a specific hypothesis formulated? How would you write the null and alternative hypotheses?
Methods
4. How were patients selected for inclusion in this study? What were the exclusion criteria?
5. In general, what are the advantages of a prospectively designed study? What are the disadvantages?
6. How did the authors attempt to limit potential biases?
7. What was the reference standard to which the imaging results were compared?
Results
8. Fifty-five patients were excluded from the study because they declined surgery. How might this influence the authors’ results?
9. How are positive predictive value and negative predictive value calculated? What is the clinical utility of a high negative predictive value?
10. The authors noted that papillomas and radial scars diagnosed at core needle biopsy had a high negative predictive value. What may be a
reason for such findings?
Physics
11. Briefly explain how dynamic signal intensity-time curves are created. What is the clinical utility of such curves?
Discussion
12. What are the study limitations? How did the authors address the study limitations? How would you design a similar study to overcome
these limitations?
Background Reading
1. Georgian-Smith D, Lawton TJ. Controversies on the management of high-risk lesions at core biopsy from a radiology/pathology perspective. Radiol Clin North Am
2010; 48:999–1012
2. Pediconi F, Padula S, Dominelli V, et al. Role of breast MR imaging for predicting malignancy of histologically borderline lesions diagnosed at core needle biopsy:
prospective evaluation. Radiology 2010; 257:653–661
F O R YO U R I N F O R M AT I O N
For more information on Journal Clubs, see “Evidence-Based Radiology A Primer in Reading Scientific Articles” in the
July 2010 AJR at www.ajronline.org/cgi/content/full/195/1/W1
*Please note that the authors of the Study Guide are distinct from those of the companion article.
280 AJR:198, February 2012This article has been cited by:
1. Manisha Bahl. 2021. Management of High-Risk Breast Lesions. Radiologic Clinics of North America 59:1, 29-40. [Crossref]
2. Mariam N. Shehata, Habib Rahbar, Meghan R. Flanagan, Mark R. Kilgore, Christoph I. Lee, Marc D. Ryser, Kathryn P.
Lowry. 2020. Risk for Upgrade to Malignancy After Breast Core Needle Biopsy Diagnosis of Lobular Neoplasia: A Systematic
Review and Meta-Analysis. Journal of the American College of Radiology 17:10, 1207-1219. [Crossref]
3. Xiaona Li, Huan Wang, Zhe Sun, Chuifeng Fan, Feng Jin, Xiaoyun Mao. 2020. A retrospective observational study of intraductal
breast papilloma and its coexisting lesions: A real‐world experience. Cancer Medicine 9:20, 7751-7762. [Crossref]
Downloaded from www.ajronline.org by 213.4.31.4 on 01/26/21 from IP address 213.4.31.4. Copyright ARRS. For personal use only; all rights reserved
4. Valeria Bertani, Martina Urbani, Manuela La Grassa, Luca Balestreri, Nicole Berger, Thomas Frauenfelder, Andreas Boss,
Magda Marcon. 2020. Atypical ductal hyperplasia: breast DCE-MRI can be used to reduce unnecessary open surgical excision.
European Radiology 30:7, 4069-4081. [Crossref]
5. Shaza Alsharif, Ann Aldis, Ahmad Subahi, Mona El Khoury, Benoit Mesurolle. 2020. Breast MRI Does Not Help
Differentiating Radial Scar With and Without Associated Atypia or Malignancy. Canadian Association of Radiologists Journal
50, 084653712093036. [Crossref]
6. Yoav Amitai, Anabel Scaranelo, Tehillah S. Menes, Rachel Fleming, Supriya Kulkarni, Sandeep Ghai, Vivianne Freitas.
2020. Can breast MRI accurately exclude malignancy in mammographic architectural distortion?. European Radiology 30:5,
2751-2760. [Crossref]
7. Sheila Boateng, Nikki Tirada, Gauri Khorjekar, Stephanie Richards, Olga Ioffe. 2020. Excision or Observation: The Dilemma
of Managing High-Risk Breast Lesions. Current Problems in Diagnostic Radiology 49:2, 124-132. [Crossref]
8. Alana A. Lewin, Cecilia L. Mercado. 2020. Atypical Ductal Hyperplasia and Lobular Neoplasia: Update and Easing of
Guidelines. American Journal of Roentgenology 214:2, 265-275. [Abstract] [Full Text] [PDF] [PDF Plus]
9. Simone Schiaffino, Massimo Calabrese, Enrico Francesco Melani, Rubina Manuela Trimboli, Andrea Cozzi, Luca Alessandro
Carbonaro, Giovanni Di Leo, Francesco Sardanelli. 2020. Upgrade Rate of Percutaneously Diagnosed Pure Atypical Ductal
Hyperplasia: Systematic Review and Meta-Analysis of 6458 Lesions. Radiology 294:1, 76-86. [Crossref]
10. Julia Bacci, Gaëtan MacGrogan, Léonie Alran, Gabrielle Labrot‐Hurtevent. 2019. Management of radial scars/complex
sclerosing lesions of the breast diagnosed on vacuum‐assisted large‐core biopsy: is surgery always necessary?. Histopathology
75:6, 900-915. [Crossref]
11. Giulia Bicchierai, Jacopo Nori, Diego De Benedetto, Cecilia Boeri, Ermanno Vanzi, Simonetta Bianchi, Maninderpal Kaur Gill,
Donatello Cirone, Vittorio Miele. 2019. Role of contrast-enhanced spectral mammography in the post biopsy management of
B3 lesions: Preliminary results. Tumori Journal 105:5, 378-387. [Crossref]
12. Emilia Josefa Borromeo Diego. Benign Breast Tumors 17-38. [Crossref]
13. Christiane K. Kuhl, Annika Keulers, Kevin Strobel, Hannah Schneider, Nadine Gaisa, Simone Schrading. 2018. Not all
false positive diagnoses are equal: On the prognostic implications of false-positive diagnoses made in breast MRI versus in
mammography / digital tomosynthesis screening. Breast Cancer Research 20:1. . [Crossref]
14. Su Min Ha, Joo Hee Cha, Hee Jung Shin, Eun Young Chae, Woo Jung Choi, Hak Hee Kim, Ha-Yeon Oh. 2018. Radial scars/
complex sclerosing lesions of the breast: radiologic and clinicopathologic correlation. BMC Medical Imaging 18:1. . [Crossref]
15. Shannon Gulla, Rachael Lancaster, Jennifer De Los Santos. 2018. High-Risk Breast Lesions and Current Management.
Seminars in Roentgenology 53:4, 252-260. [Crossref]
16. Lars J. Grimm, Christine E. Bookhout, Rex C. Bentley, Sheryl G. Jordan, Thomas J. Lawton. 2018. Concordant, non-atypical
breast papillomas do not require surgical excision: A 10-year multi-institution study and review of the literature. Clinical
Imaging 51, 180-185. [Crossref]
17. Yoav Amitai, Tehillah Menes, Orit Golan. 2018. Use of Breast Magnetic Resonance Imaging in Women Diagnosed with Atypical
Ductal Hyperplasia at Core Needle Biopsy Helps Select Women for Surgical Excision. Canadian Association of Radiologists
Journal 69:3, 240-247. [Crossref]
18. Jill Hammersley, Savannah Partridge, Grace Blitzer, Sarah Deitch, Habib Rahbar. 2018. Management of high-risk breast lesions
found on mammogram or ultrasound: the value of contrast-enhanced MRI to exclude malignancy. Clinical Imaging . [Crossref]
19. Megan E. Sullivan. New Thoughts on Atypias of the Breast: Flat Epithelial Atypia, Atypical Ductal Hyperplasia, and Lobular
Neoplasia 117-126. [Crossref]
20. Giulia Bicchierai, Jacopo Nori, Francesco Amato. High-Risk (B3) Lesions 169-184. [Crossref]21. Keiko Tsuchiya, Naoko Mori, David V. Schacht, Deepa Sheth, Gregory S. Karczmar, Gillian M. Newstead, Hiroyuki Abe.
2017. Value of breast MRI for patients with a biopsy showing atypical ductal hyperplasia (ADH). Journal of Magnetic Resonance
Imaging 46:6, 1738-1747. [Crossref]
22. Michael A. Cohen, Mary S. Newell. 2017. Radial Scars of the Breast Encountered at Core Biopsy: Review of Histologic,
Imaging, and Management Considerations. American Journal of Roentgenology 209:5, 1168-1177. [Abstract] [Full Text] [PDF]
[PDF Plus]
23. Savitri Krishnamurthy, Therese Bevers, Henry M. Kuerer, Benjamin Smith, Wei Tse Yang. 2017. Paradigm Shifts in Breast Care
Delivery: Impact of Imaging in a Multidisciplinary Environment. American Journal of Roentgenology 208:2, 248-255. [Abstract]
Downloaded from www.ajronline.org by 213.4.31.4 on 01/26/21 from IP address 213.4.31.4. Copyright ARRS. For personal use only; all rights reserved
[Full Text] [PDF] [PDF Plus]
24. BRIAN ORR, JOSEPH L. KELLEY. 2016. Benign Breast Diseases: Evaluation and Management. Clinical Obstetrics &
Gynecology 59:4, 710-726. [Crossref]
25. Elizabeth Tágide Kalife, Ana P. Lourenco, Grayson L. Baird, Yihong Wang. 2016. Clinical and Radiologic Follow-up Study for
Biopsy Diagnosis of Radial Scar/Radial Sclerosing Lesion without Other Atypia. The Breast Journal 22:6, 637-644. [Crossref]
26. Barbara Bennani-Baiti, Nabila Bennani-Baiti, Pascal A. Baltzer. 2016. Diagnostic Performance of Breast Magnetic Resonance
Imaging in Non-Calcified Equivocal Breast Findings: Results from a Systematic Review and Meta-Analysis. PLOS ONE 11:8,
e0160346. [Crossref]
27. Taffurelli M, Pellegrini A, Ghignone F, Santini D, Zanotti S, Serra M. 2016. Positive predictive value of breast lesions of
uncertain malignant potential (B3): Can we identify high risk patients? The value of a multidisciplinary team and implications
in the surgical treatment. Surgical Oncology 25:2, 119-122. [Crossref]
28. Kandice K. Ludwig. Proliferative Breast Disease 59-79. [Crossref]
29. Benjamin C Calhoun, Laura C Collins. 2016. Recommendations for excision following core needle biopsy of the breast: a
contemporary evaluation of the literature. Histopathology 68:1, 138-151. [Crossref]
30. Emilia Josefa Borromeo Diego. Benign Breast Tumors 23-56. [Crossref]
31. Cathleen Matrai, Timothy M. D'Alfonso, Lindsay Pharmer, Michele B. Drotman, Rache M. Simmons, Sandra J. Shin. 2015.
Advocating Nonsurgical Management of Patients With Small, Incidental Radial Scars at the Time of Needle Core Biopsy: A
Study of 77 Cases. Archives of Pathology & Laboratory Medicine 139:9, 1137-1142. [Crossref]
32. R. Jared Weinfurtner, Bhavika Patel, Christine Laronga, Marie C. Lee, Shannon L. Falcon, Blaise P. Mooney, Binglin Yue,
Jennifer S. Drukteinis. 2015. Magnetic Resonance Imaging-Guided Core Needle Breast Biopsies Resulting in High-Risk
Histopathologic Findings: Upstage Frequency and Lesion Characteristics. Clinical Breast Cancer 15:3, 234-239. [Crossref]
33. Aziza Nassar, Amy L. Conners, Betul Celik, Sarah M. Jenkins, Carin Y. Smith, Tina J. Hieken. 2015. Radial scar/complex
sclerosing lesions: a clinicopathologic correlation study from a single institution. Annals of Diagnostic Pathology 19:1, 24-28.
[Crossref]
34. Theresa Schwartz, Amy Cyr, Julie Margenthaler. 2014. Screening breast magnetic resonance imaging in women with atypia or
lobular carcinoma in situ. Journal of Surgical Research . [Crossref]
35. Meroni Stefano, Bozzini Anna Carla, Pruneri Giancarlo, Moscovici Oana Codrina, Maisonneuve Patrick, Menna Simona, Penco
Silvia, Meneghetti Lorenza, Renne Giuseppe, Cassano Enrico. 2014. Underestimation rate of lobular intraepithelial neoplasia
in vacuum-assisted breast biopsy. European Radiology 24:7, 1651-1658. [Crossref]
36. Pierre-Emmanuel Colombo, Anne Vincent-Salomon, Marie-Christine Chateau, Anne Mourregot, Marian Gutowski, Guillaume
Laffargue, Bruno Masson, Aurélie Maran-Gonzalez, Philippe Rouanet. 2014. Quelle prise en charge chirurgicale pour « les
lésions à haut risque » de cancer du sein ?. Bulletin du Cancer 101:7-8, 718-729. [Crossref]
37. Cynthia L. Miller, Jane A. West, Anna C. Bettini, Frederick C. Koerner, Thomas M. Gudewicz, Phoebe E. Freer, Suzanne B.
Coopey, Michele A. Gadd, Kevin S. Hughes, Barbara L. Smith, Elizabeth Rafferty, Michelle C. Specht. 2014. Surgical excision
of radial scars diagnosed by core biopsy may help predict future risk of breast cancer. Breast Cancer Research and Treatment
145:2, 331-338. [Crossref]
38. Amène Aissa, Majdi Ben Lassoued, Rafika Alouini. 2014. Microbiopsie mammaire : fiabilité en fonction du BIRADS. Imagerie
de la Femme 24:1, 1-13. [Crossref]
39. B. Boyer, E. Russ. 2014. Corrélations anatomoradiologiques : distorsions architecturales. Journal de Radiologie Diagnostique et
Interventionnelle 95:2, 136-144. [Crossref]
40. B. Boyer, E. Russ. 2014. Anatomical-radiological correlations: Architectural distortions. Diagnostic and Interventional Imaging
95:2, 134-140. [Crossref]41. E.S. Buckley, F. Webster, J.E. Hiller, D.M. Roder, G. Farshid. 2014. A systematic review of surgical biopsy for LCIS found at
core needle biopsy – Do we have the answer yet?. European Journal of Surgical Oncology (EJSO) 40:2, 168-175. [Crossref]
42. Samantha L. Heller, Kristin Elias, Avani Gupta, Heather I. Greenwood, Cecilia L. Mercado, Linda Moy. 2014. Outcome
of High-Risk Lesions at MRI-Guided 9-Gauge Vacuum- Assisted Breast Biopsy. American Journal of Roentgenology 202:1,
237-245. [Abstract] [Full Text] [PDF] [PDF Plus]
43. Karen Kinkel. MRI of the Breast: Current Indications and Outlook to the Future 319-322. [Crossref]
44. Samantha L. Heller, Ozvaldo Hernandez, Linda Moy. 2013. Radiologic-pathologic Correlation at Breast MR Imaging. Magnetic
Downloaded from www.ajronline.org by 213.4.31.4 on 01/26/21 from IP address 213.4.31.4. Copyright ARRS. For personal use only; all rights reserved
Resonance Imaging Clinics of North America 21:3, 583-599. [Crossref]
45. Christopher P. Ho, Jennifer E. Gillis, Kristen A. Atkins, Jennifer A. Harvey, Brandi T. Nicholson. 2013. Interactive Case
Review of Radiologic and Pathologic Findings from Breast Biopsy: Are They Concordant? How Do I Manage the Results?.
RadioGraphics 33:4, E149-E152. [Crossref]
46. M. Castro Barba, M.P. Cobos Bombardiere, A. Wernicke, N. Lonegro, C. Cravero, F. Sarquis. 2013. Manejo de las lesiones
mamarias de alto riesgo diagnosticadas mediante biopsia percutánea. Revista Argentina de Radiología 77:4, 284-290. [Crossref]
47. Ying Zhu, Shuping Zhang, Peifang Liu, Hong Lu, Yilin Xu, Wei T. Yang. 2012. Solitary Intraductal Papillomas of the Breast:
MRI Features and Differentiation From Small Invasive Ductal Carcinomas. American Journal of Roentgenology 199:4, 936-942.
[Abstract] [Full Text] [PDF] [PDF Plus]
48. Chiara Zuiani, Viviana Londero, Anna Linda, Rossano Girometti, Massimo Bazzocchi. 2012. MRI in B3 lesions, low grade
DCIS, high DCIS: is MR selecting the dangerous cases?. European Journal of Radiology 81, S189-S191. [Crossref]
49. Anna Linda, Chiara Zuiani, Viviana Londero, Massimo Bazzocchi. 2012. What to do with B3 lesions at needle biopsy. European
Journal of Radiology 81, S90-S92. [Crossref]
50. Viviana Londero, Chiara Zuiani, Anna Linda, Rossano Girometti, Massimo Bazzocchi, Francesco Sardanelli. 2012. High-Risk
Breast Lesions at Imaging-Guided Needle Biopsy: Usefulness of MRI for Treatment Decision. American Journal of Roentgenology
199:2, W240-W250. [Abstract] [Full Text] [PDF] [PDF Plus]
51. Jisun Kim, Wonshik Han, Eun-Young Go, Hyeong-Gon Moon, Soo Kyung Ahn, Hee-Chul Shin, Jee-Man You, Jung Min
Chang, Nariya Cho, Woo Kyung Moon, In Ae Park, Dong-Young Noh. 2012. Validation of a Scoring System for Predicting
Malignancy in Patients Diagnosed with Atypical Ductal Hyperplasia Using an Ultrasound-Guided Core Needle Biopsy. Journal
of Breast Cancer 15:4, 407. [Crossref]You can also read
