Invasive cribriform carcinoma of the breast: mammographic,sonographic,MRI,and 18 F-FDG PET-CT features

Abstract

Background

Invasive cribriform carcinoma (ICC) of the breast is a rare type of invasive carcinoma which shows a favorable prognosis and a lower frequency of axillary nodal metastases. Few imaging findings related to ICC have been reported.

Purpose

To evaluate imaging findings with multiple imaging techniques in ICC of the breast.

Material and Methods

Twenty-eight cases of histopathologically proven ICC of the breast were gathered for this study. We retrospectively reviewed the mammographic, sonographic, and magnetic resonance imaging (MRI) findings of ICC according to the American College of Radiology (ACR) breast imaging reporting and data system (BI-RADS) lexicon. 18 F-fluorodeoxyglucose positron emission tomography-computed tomography (18 F-FDG PET-CT) findings were also evaluated. Microscopic slides of surgical specimens were reviewed by a breast pathologist.

Results

The mean age of the patients was 51 years. The most common mammographic findings were irregular shape (72.8%), spiculated margin (63.7%), and a high density (81.8%) mass. Microcalcifications were noted in 9/28 cases. The most common shape was pleomorphic (66.7%). The most common sonographic findings were irregular shape (77.8%), spiculated margin (29.6%), hypoechogenicity (81.5%), and no posterior acoustic features (85.2%). On MRI, most ICCs presented as irregular shaped mass (62.0%) and irregular (42.9%) margin. All four patients (16.0%) who presented with non-mass-like enhancement pattern showed a segmental distribution. The 18 F-FDG PET-CT showed a mean maximum standardized uptake value (SUVmax) of 5.90. Axillary nodal metastases were found in 17.9% (5/28) of the surgical specimens. Immunohistochemical studies showed a high positivity for estrogen and progesterone receptor (100% and 87.5%, respectively).

Conclusion

The imaging features of invasive cribriform carcinoma are highly suggestive of malignancy and are not distinguishable from those of other breast cancers like infiltrating ductal carcinoma.

Keywords

Breast neoplasms – primary mammography ultrasound magnetic resonance imaging (MRI)positron emission tomography (PET)

Introduction

Invasive cribriform carcinoma (ICC) is an unusual type of primary breast carcinoma that is composed of predominantly cribriform invasive components (1,2). In 1983, Page et al. initially described a separate histological type of breast carcinoma upon reviewing the histology and clinical data of 1003 invasive breast carcinomas (1). It was characterized as having a more favorable prognosis than ordinary breast carcinoma, and axillary node metastasis were uncommon (1,3,4).

To the best of our knowledge, radiological reports on their imaging characteristics are limited because ICCs occur infrequently only. Previous studies consist of two case reports and two retrospective studies (5 –8). The number of previously reported cases was low and the studies reported various findings on mammography, sonography, and magnetic resonance imaging (MRI). The purpose of this study was to investigate whole-breast imaging findings of ICC, including mammography, sonography, MRI, and 18 F-fluorodeoxyglucose positron emission tomography-computed tomography (18 F-FDG PET-CT).

Material and Methods

Thirty-six patients with invasive cribriform carcinoma were identified in our computerized pathology database between July 2006 and February 2013. Five patients were excluded because the final pathologic diagnosis of the specimen was infiltrating ductal carcinoma (IDC), despite being confirmed as ICC on core-needle biopsy. Three more patients were excluded because radiologic images were not available. In total, 28 patients were included in this study.

By mammography, craniocaudal and mediolateral oblique views were obtained using a Mammomat 3000 (Siemens Medical Solutions, Solna, Sweden) and Lorad M3 (Hologic Inc., Boston, MA, USA) mammography unit. Parenchymal patterns on mammograms were categorized as one of the following: almost entirely fatty; scattered fibroglandular tissue; heterogeneously dense; extremely dense. Each mammographic lesion was analyzed for mass characteristics (i.e. shape, margin, density), presence of architectural distortion, and the type of microcalcification according to the American College of Radiology (ACR) breast imaging reporting and data system (BI-RADS) lexicon.

Ultrasound (US) was performed using a HDI 5000 (Advanced Technology Laboratories, Bothell, WA, USA) or IU22 (Philips Ultrasound, Bothell, WA, USA) US systems with a 5–12 MHz linear probe. We examined both breasts and the axillary lymph nodes. US imaging findings were reviewed for shape, orientation, margin, boundary, echogenicity, posterior acoustic features, and associated calcifications, and categorized according to the ACR BI-RADS final assessment. The largest diameter obtained from either the sagittal or transverse views was recorded as the maximum tumor diameter. On the basis of previous studies, we defined the presence of axillary lymph node metastasis on US when the lymph node had at least one of these findings: a mean longitudinal-transverse axis ratio of less than 1.5, presence of eccentric cortical thickening, or loss of a central fatty hilum (9).

MRI was performed using a 1.5-T scanner (Signa Excite, GE Healthcare, Milwaukee, WI, USA) equipped with a breast coil. Images were acquired in axial plane with the following sequences: axial, T2-weighted, fat-suppressed, fast spin-echo imaging (TR/TE, 5000/86; flip angle, 90°; field of view [FOV], 300 mm; acquisition matrix, 256 × 256; number of excitations (NEX), 3; slice thickness, 4.5 mm); pre- and postcontrast, axial, T1-weighted (T1W) three-dimensional (3D) fast spoiled gradient-recalled echo sequence with parallel volume imaging (VIBRANT, GE Healthcare) (TR/TE, 6.5/3.1; flip angle, 10°; FOV, 300 mm; acquisition matrix, 350 × 350; NEX, 1; slice thickness, 1.1 mm). Gadodiamide (Omniscan, GE Healthcare, Oslo, Norway) was administered as contrast agent with an intravenous bolus injection (0.2 mmol per kg of body weight) at 3 mL/s. Imaging was performed before the intravenous contrast agent bolus injection and four times after this injection for a period of 7.3 min. The image postprocessing, included the subtraction of unenhanced images from enhanced images, sagittal reformations, and 3D maximum-intensity projections by using the first contrast-enhanced series. The interpretation of the degree and patterns of enhancement was performed by visual assessment. Associated findings were recorded, such as nipple retraction, skin thickening, lymphadenopathy, hematoma, and invasion of the pectoralis muscle or chest wall.

All mammograms, sonograms, and MR images were retrospectively reviewed in consensus by one radiologist with 6 years of experience in breast imaging and by one resident.

18 F-FDG PET-CT imaging was performed using a Discovery ST-16 system (GE Healthcare, Milwaukee, WI, USA). Normal fasting blood glucose levels (after fasting for at least 6 h) were determined to be <150 mg/dl for all patients. All patients ingested more than 500 mL of fluid for adequate urination. An intravenous injection of 8.14 MBq/kg (0.22 mCi/kg) of FDG was then given and the subjects rested for approximately 1 h. Precontrast CT scanning was performed using a 16-channel CT from the skull base to the upper thigh prior to PET. PET was then immediately conducted over the same body region using five to seven bed positions with a 3-min acquisition time per bed position. The CT data were used for attenuation correction and anatomical correlation with the PET data. All data were evaluated on a workstation (Advanced workstation, version 4.3, GE Healthcare) by an experienced nuclear medicine physician and a resident in consensus. The PET scans were visually and semi-quantitatively analyzed. The FDG uptake was considered to be abnormal on visual analysis when the uptake in the region of the primary tumor was substantially higher than the background uptake in the contralateral breast or axilla. The highest recorded FDG uptake was semi-quantitatively analyzed after being corrected for radioactive decay, according to the following formula: maximum standardized uptake value (SUVmax) = mean region of interest activity (mCi/mL) / injected dose (mCi) / body weight (g).

The histopathologic diagnosis was confirmed by core-needle biopsy, excision biopsy, lumpectomy, or mastectomy. The surgical specimen was considered as the gold standard if both, core-needle or excision biopsy, and surgery were performed. Excision biopsy and core-needle biopsy were considered as the gold standard if no surgery was performed. The slides for microscopic examination of the specimens were reviewed by one experienced breast pathologist. Axillary lymph node metastasis was evaluated from the dissected lymph node specimen, including the sentinel axillary lymph node. The histological grading of the tumor was performed according to the Elston and Ellis protocol (10). This involves the assessment of three components of tumor morphology; we performed immunohistochemical studies for estrogen receptor (ER) and progesterone receptor (PR) in this study. The status of ER and PR were evaluated according to the American Society of Clinical Oncology/College of American Pathologists (ASCO/CAP) guidelines for immunohistochemistry. ER and PR are considered positive if there are at least 1% positive tumor nuclei.

An independent samples T test was used to identify the relationship between microcalcification and the percentage of DCIS component. A P value of 0.05 or less was considered to indicate a statistically significant difference. SPSS for Microsoft Windows software (version 18.0, SPSS Inc., Chicago, IL, USA) was used for the statistical data analysis.

Results

The mean age of the 28 patients was 51 years (range, 32–70 years).

Of the 28 patients, 27 underwent preoperative mammography. The breast parenchyma comprised almost entirely of fatty breast tissue in two patients, scattered fibroglandular tissue in eight patients, heterogeneously dense breast tissue in 14 patients, and extremely dense breast tissue in three patients.

The characteristics of the masses are summarized in Table 1.

Table 1.

Mammographic characteristics of invasive cribriform carcinoma.

Findings (n = 27)	n (%)
Negative	3 (11.1)
Mass only	14 (51.9)
Mass with calcifications	8 (29.6)
Focal asymmetry	1 (3.7)
Calcification only	1 (3.7)
Mass shape (n = 22)
Round	3 (13.6)
Oval	3 (13.6)
Irregular	16 (72.8)
Mass margin (n = 22)
Circumscribed	3 (13.6)
Microlobulated	5 (22.7)
Spiculated	14 (63.7)
Mass density (n = 22)
High	18 (81.8)
Equal	4 (18.2)
Shape of associated microcalcifications (n = 9)
Round	1 (11.1)
Amorphous	1 (11.1)
Dystrophic	1 (11.1)
Pleomorphic	6 (66.7)
Distribution of microcalcifications (n = 9)
Regional	1 (11.1)
Clustered	7 (77.8)
Segmental	1 (11.1)

Of the 27 patients with preoperative mammograms, 22 had tumors that presented as masses. According to the ACR BI-RADS lexicon, the most common findings presenting as masses had irregular shape (72.8%), spiculated margins (63.7%), and high density (81.8%) (Fig. 1a). Microcalcifications were present within the mass in 36.4% (8/22) of cases. The most common shape of the microcalcifications was pleomorphic in five cases (62.5%) (Fig. 2a). One patient had microcalcifications only without mass or asymmetry (3.7%), presenting with pleomorphic shape and clustered distribution.

Fig. 1.

An invasive cribriform carcinoma in a 49-year-old woman who presented with a palpable mass in the right breast. (a) Craniocaudal and mediolateral oblique mammograms of the right breast show an extremely dense breast. There is an irregular, spiculated high-density 3.7 cm mass at the 9 o’clock position of the right breast (arrows). An enlarged lymph node (arrowhead) with eccentric cortical thickening is seen at the ipsilateral axillary area on the mediolateral oblique view. (b) Sonography of the right breast shows an irregular, spiculated, hypoechoic mass with echogenic echo boundary at the 9 o’clock direction (arrow). (c) Axial, contrast-enhanced T1W MRI of the right breast reveals an irregular inhomogeneous enhancing mass at the 9 o’clock position (arrow). (d) 18 F-FDG PET maximum intensity projection (MIP) image shows a subtle increased glucose metabolism (SUVmax = 4.6) in the right breast. The right axillary lymph node is not seen at this image. (e) Microscopic specimen (hematoxylin-eosin, original magnification x 100) shows a cribriform pattern with apparent tubular structures. Foci of elastosis (arrow) are present.

Fig. 2.

An invasive cribriform carcinoma in a 65-year-old woman who presented with a palpable mass in the right breast. (a) Craniocaudal and mediolateral oblique mammograms of the right breast show an almost entirely fatty breast. There is an approximately 3.0 cm conglomerate of irregular, spiculated, high density masses (arrows) associated with multiple segmental distributed pleomorphic microcalcifications (arrowheads) at the 12 o’clock position of the right breast. (b) Sonography of the right breast shows conglomerated hypoechoic masses with irregular shape, angular margin, and echogenic echo boundary at the 12 o’clock direction (arrow). Note the microcalcifications (arrowheads) within the mass.

Ultrasonography was performed in 27 patients (Table 2) and masses were found in all 27 patients. Following characteristics of the masses were most commonly found: irregular shape in 21 patients (77.8%), spiculated margin in eight patients (29.6%), parallel orientation in 21 patients (77.8%), abrupt interface at the lesion boundary in 17 patients (63.0%), and hypoechogenicity in 22 patients (81.5%). Four patients (14.8%) were suspected of having axillary lymph node metastasis and all of them were confirmed to have lymph node metastasis on the dissected lymph node specimens. One patient with negative axillary lymph nodes on US had lymph node metastasis on pathological examination.

Table 2.

Sonographic characteristics of invasive cribriform carcinoma.

Findings (n = 27)	n (%)
Shape
Oval	4 (14.8)
Round	2 (7.4)
Irregular	21 (77.8)
Margin
Circumscribed	2 (7.4)
Microlobulated	5 (18.5)
Angular	7 (26.0)
Indistinct	5 (18.5)
Spiculated	8 (29.6)
Echo pattern
Hypoechoic	22 (81.5)
Isoechoic	2 (7.4)
Mixed echoic	3 (11.1)
Orientation
Parallel	21 (77.8)
Not parallel	6 (22.2)
Lesion boundary
Abrupt interface	17 (63.0)
Echogenic halo	10 (37.0)
Posterior acoustic features
No posterior acoustic features	23 (85.2)
Posterior acoustic enhancement	2 (7.4)
Posterior shadowing	1 (3.7)
Combined pattern	1 (3.7)

Twenty-five of the 28 patients with ICC underwent breast MRI (Table 3). Most patients had distinct masses (84.0%, 21/25), and a non-mass-like enhancement with segmental distribution was found in four patients (16.0%) (Fig. 3). Of the 21 tumors with breast masses, 13 had an irregular mass (62.0%), four had an oval mass (19.0%) and four had a lobular mass (19.0%). The margins were irregular (42.9%) or spiculated (33.3%) for most masses (Fig. 1c).

Fig. 3.

An invasive cribriform carcinoma in a 38-year-old woman. Axial, contrast-enhanced T1W MRI of the right breast reveals an approximately 5.0 cm extented non-mass-like enhancement with segmental distribution and extension to the right nipple at the right upper outer quadrant (arrow).

Table 3.

MRI characteristics of invasive cribriform carcinoma.

Findings (n = 25)	n (%)
Mass	21 (84.0)
Mass shape (n = 21)
Oval	4 (19.0)
Lobular	4 (19.0)
Irregular	13 (62.0)
Mass margin (n = 21)
Smooth	5 (23.8)
Irregular	9 (42.9)
Spiculated	7 (33.3)
Non-mass-like enhancement	4 (16.0)
Distribution of non-mass (n = 4)
Segmental	4 (100.0)

18F-FDG PET-CT was performed in 23 patients (Table 4). FDG uptake was noted in 20 patients (87.0%) and no FDG uptake was seen in four patients (13.0%). The mean SUVmax value was 5.90 (range, 1.2–14.3) in the 20 patients with FDG uptake (Fig. 1d). There were no distant metastases shown by 18 F-FDG PET-CT.

Table 4.

18F-FDG PET-CT characteristics of invasive cribriform carcinoma.

Findings (n = 23)	n (%)
FDG uptake
Positive	20 (87.0)
Negative	3 (13.0)
Mean SUVmax	5.90
Lymph node uptake	3 (13.0)

The final pathologic diagnosis was obtained by lumpectomy in 16 patients, mastectomy in eight patients, excision biopsy in one patient, and core-needle biopsy in three patients. The final histopathologic diagnosis of all patients was pure invasive cribriform carcinoma (Fig. 1e). Of the 24 surgical specimens, all cases were grade 1 (low-grade) tumors and axillary nodal metastases were identified in five patients (17.9%). The immunohistochemical profile was positive for ER (100%, 24/24) and PR (87.5%, 21/24).

Discussion

Histologically, invasive breast carcinomas are subdivided into infiltrating ductal carcinoma (IDC) and “special types” such as invasive lobular carcinoma, medullary carcinoma, mucinous carcinoma, et cetera. IDC is the most common type of invasive breast cancer. ICC is one of these “special types” and an unusual type of breast carcinoma. The incidence of ICC is about 0.3–6% of primary breast carcinomas (1,3,4). According to Page et al., ICC is divided into two groups; the “classical” type that shows predominantly cribriform elements with or without a limited amount of tubular invasive elements (less than 50%) and the “mixed” type with more than 50% of invasive cribriform pattern containing areas of less well differentiated invasive carcinoma (2). According to previous reports, the classical type of ICC shows a more favorable prognosis with a lower degree of lymph node involvement than the mixed type of ICC and IDC (1 –3).

In this study, we found that ICC had malignant imaging characteristics similar to IDC in radiologic and PET-CT imaging, even though ICC has a lower malignant grade and a more favorable prognosis than IDC (11,12). There are only few reports describing the radiologic findings of ICC (5 –8).

Stutz et al. reported mammographic findings in eight cases and sonographic findings in four cases (5). On mammography, 50% (4/8) of cases appeared as a spiculated mass. Three of four cases (75%) had ill-defined and inhomogeneous masses by ultrasonography. Nishimura et al. reported one case of ICC in a man. It was a circumscribed marginated high-density mass with microcalcifications on mammography (6). As reported by Lim et al., three cases appeared with an oval or irregular shape, partially microlobulated or well-circumscribed margins, and a hypoechoic or anechoic mass on sonographic findings (7). The above-mentioned studies reported various findings on mammography and US and these findings were mostly suspicious of malignancy. In our study, the most findings suspicious of malignancy presented with irregular shape (72.8% on mammography and 77.8% on sonography) and spiculated margins (63.7% on mammography and 29.6% on sonography) (Tables 1 and 2).

Tumor margins seen on sonography may reflect the histological grade of invasive cancers. There are several recent publications about the ultrasonographic imaging findings according to the histological grade of infiltrating ductal carcinoma (13 –16). According to these studies, high-graded malignant lesions are more likely to have microlobulated margins, abrupt boundary, and a posterior acoustic enhancement. Low and intermediate graded tumors tend to present with indistinct or spiculated margins because of the low degree of desmoplastic reactions in high grade tumors. In our study, most margins were spiculated on both mammography and sonography. The histological grade of all ICC was grade 1 (well differentiated). This finding in ICC probably indicates the low and intermediate grade nature of this tumor with desmoplastic reaction.

On mammography, microcalcifications were seen in 33.3% (9 of 27) of the patients. 77.8% of the patients (21/27) showed DCIS components associated with ICC at the histopathologic examination of the surgical specimens, except in the three cases where a core-needle biopsy was performed only. Of the nine patients with microcalcifications, seven (77.8%) had DCIS components at the histopathologic examination. There was no significant relationship between the DCIS component and the microcalcifications within the tumor (P > 0.05). Accordingly, we found that the microcalcification in ICC should not to be related to DCIS components.

An irregular shaped and irregular marginated mass was the most common MRI appearance in our study. So far, the MRI features of ICC have been described in one case only (7). Lim et al. reported that ICC displayed an oval shaped mass with homogenous early enhancement and delayed washout pattern based on the kinetic curve analysis (7). In the present study, the four remaining patients presented with a non-mass-like enhancement with segmental distribution (16.0%). Of those four patients, only three patients underwent surgery. In those patients, the mean extent of the primary lesion was 5.0 cm (range, 4.7–5.3 cm) at MRI. The histopathology report revealed that approximately 43.3% of the DCIS was associated with invasive cancer. The mean histologic size of the invasive carcinoma was 1.1 cm (range, 0.9–1.3 cm), which was smaller than the extent of the primary lesion at MRI. Previous studies explained that DCIS have a high relationship with non-mass-like enhancement (17 –19). We postulate the different MRI presentation such as the non-mass-like enhancement may be primarily due to DCIS components.

We also investigated the 18 F-FDG PET-CT images of ICCs, which has not been reported yet. In our study, 87.0% (20/23) of lesions showed FDG uptake. Many published studies with preoperative 18 F-FDG PET-CT in patients with primary breast carcinoma have suggested that higher levels of FDG uptake are significantly correlated with a poor prognosis, similar tumor invasiveness (>2 cm), higher histological grade, negative hormonal receptor status, axillary lymph node metastasis, and histological type of primary breast carcinoma (IDC in comparison with invasive lobular carcinoma [ILC]) (20 –26). Primary breast cancers with FDG high uptake (range, 4.1–7.4) are considered to have poor prognosis compared to those with low FDG uptake (range, 2.8–5.2) (27 –30). The mean SUVmax value of the primary tumor was 5.90 (range, 1.2–14.3) in the present study. Compared with the aforementioned reports, our result of ICC showed relatively higher values, even though ICC has a favorable prognosis and a well-differentiated tumor.

False negative results were found in 13% (3 of 23) of the patients. The false negative rate by PET-CT has been reported to be 23.7–46.5% in IDC and 60–65.2% in ILC (29,30). Low sensitivity was described for the detection of small lesions (≤10 mm) and lower histological grades on FDG PET in patients with primary breast carcinoma (30). The authors explained that a high rate of false negative result in ILC was affected by different microscopic growth pattern, such as lower tumor cell density and diffuse infiltration of the surrounding tissue (26,27,29). In our study, the tumor size was smaller than 1 cm and the histological grade was also well-differentiated in three patients with false negative findings. We postulate these factors could be a cause of false negative findings in the present study. The false negative rate of ICC in our study was relatively lower than that of IDC and ILC in previous reports (29,30). Because of the relatively small number of subjects, further research is necessary to evaluate the PET-CT findings of ICC and to compare them with IDC and ILC.

Pure ICC is characterized by lower rates of axillary lymph node involvement, higher positive rates of ER and/or PR expression than in mixed ICC and IDC (1,3,4,31). Those characteristics are one of the important prognostic factors for breast cancer. In our cases, axillary nodal metastases were identified in only five tumors (17.9%) and the expression of ER (100%) and PR (87.5%) were high. These results concur with previous publications and could be considered to support the favorable prognosis of this carcinoma (1,3,31).

As mentioned above, imaging findings of ICC are nonspecific. A histopathologic analysis through core needle biopsy or surgical resection is needed for a correct diagnosis.

This study has several limitations. First, this was a retrospective study, so not all patients underwent all four imaging studies (mammography, sonography, MRI, and 18 F-FDG PET-CT). Second, the number of study patients was small because of the rarity of this tumor. Third, the study lacks a control group composed of patients who were diagnosed with IDC. A comparison of ICC with IDC should precede an analysis of the character of ICC.

In conclusion, the imaging features of invasive cribriform carcinoma are highly suggestive of malignancy, usually presenting as an irregular and spiculated mass on mammography and sonography, an irregular enhancing mass on MRI and with a relatively higher SUVmax value on 18 F-FDG PET-CT.

Footnotes

Conflict of interest

None declared.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

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