Invasive ductolobular carcinoma of the breast: spectrum of mammographic, ultrasound and magnetic resonance imaging findings correlated with proportion of the lobular component
© Menezes et al.; licensee Springer. 2013
Received: 18 October 2013
Accepted: 21 October 2013
Published: 20 November 2013
The aim of this study was to describe the imaging features of patients with invasive ductolobular carcinoma of the breast in comparison with the proportion of the lobular component.
Materials and methods
We retrospectively reviewed mammographic, sonographic and MRI records of 113 patients with proven ductolobular carcinoma diagnosed between January 2008 and October 2012 according to the BI-RADS ® lexicon, and correlated these to the proportion of the lobular component.
At mammography the most common finding (62.9%) for invasive ductolobular carcinoma was an irregular, spiculated and isodense mass. On ultrasound an irregular and hypoechoic mass, with spiculated margins and posterior acoustic shadowing was observed in 46.8% of cases. Isolated mass and mass associated with non-mass like enhancement (NMLE) were the most common findings by MRI (89.4%). Washout pattern in delayed phase was seen in 61.2% and plateau curve was more frequently observed in patients with larger lobular component. Additional malignant findings (multifocality, multicentricity and contralateral disease) did not correlate significantly with the proportion of the lobular component.
Invasive ductolobular carcinoma mainly presents as an irregular, spiculated mass, isodense on mammography and hypoechoic with posterior acoustic shadowing. On MRI it is usually seen as an isolated mass or as a dominant mass surrounded by smaller masses or NMLE. Washout is the most ordinary kinetic pattern of these tumors. In general, the imaging characteristics did not vary significantly with the proportion of the lobular component.
KeywordsBreast carcinoma Lobular Ductal Mammography Ultrasonography Magnetic resonance imaging
Breast cancer is a heterogeneous group of tumors with multivariate morphology, growth pattern, molecular profiles and response to treatment. The majority of invasive breast cancers (72 – 80%) are categorized as invasive ductal carcinoma (IDC). The prevalence of the second most common type of breast cancer, invasive lobular carcinoma (ILC), accounts for 5 to 15% (Biglia et al. 2007; Li et al. 2003; Verkooijen et al. 2003).
There is an extensive literature on clinical and imaging characteristics of both IDC and ILC (Acs et al. 2001; Arps et al. 2013; Brem et al. 2009; Kim et al. 2011; Korhonen et al. 2004; Lopez & Bassett 2009; Sastre-Garau et al. 1996; Winston et al. 2000; Yang et al. 2007). Multiple differences in demographic and tumor features between these two histological types have been reported. Patients with ILC are generally older at the time of the diagnosis, (Sastre-Garau et al. 1996; Moran et al. 2009) ILC is usually larger in diameter, (Arpino et al. 2004; Biglia et al. 2013) is more frequently hormone receptor positive, (Arps et al. 2013; Arpino et al. 2004) has lower grade than IDC, (Arps et al. 2013; Arpino et al. 2004; Biglia et al. 2013) is more frequently multifocal, multicentric and bilateral, and the organ distribution of metastatic disease tends to spread to pelvic organs, gastrointestinal tract and also to distinct sites such as retroperitoneum, meninges, ovary and serosa.
ILC has the histological characteristic to spread in rows of single cell layers around normal ducts like a “spider web”, infiltrating the preexisting stroma without inducing a strong desmoplastic response (Michael et al. 2008; Qureshi et al. 2006). This growth pattern causes minimum disruption of the normal anatomical structures than IDC, turning the radiological and clinical diagnostic of this tumor into a real challenge (Yeatman et al. 1995). This insidiously invasive nature makes the full extent of these tumors difficult to diagnose in screening. Mammogram may only reveal subtle changes or can even be completely normal. Mammographic sensitivity for detection of ILC varies between 57-92% (Butler et al. 1999; Hilleren et al. 1991a; Le et al. 1992) and ILC has higher false negative rates than IDC (19 vs. 10%) (Framarino Dei et al. 1995), making ILC more difficult to diagnose, especially in early stage. Ultrasound (US) is slightly more sensitive than mammography (sensitivity between 68-95%) and has shown to be more accurate in determine the (pathologic) size of the lesion, and also in identifying multifocality and multicentricity (Butler et al. 1999; Berg et al. 2004; Chapellier et al. 2000; Paramagul et al. 1995; Selinko et al. 2004). Magnetic resonance imaging (MRI) has become mainstream for diagnosis and work-up of breast cancer patients and many studies have demonstrated this imaging modality to have sensitivity above 90% (Butler et al. 1999; Berg et al. 2004; Chapellier et al. 2000; Boetes et al. 1995; Boetes et al. 1997; Harms et al. 1993; Mumtaz et al. 1997; Orel et al. 1994; Orel & Schnall 2001; Peters et al. 2008; Qayyum et al. 2002; Rodenko et al. 1996). MRI plays a fundamental role in providing additional information not obtained by conventional digital mammography and ultrasound, being of great importance in recognition of ipsilateral and contralateral lesions (Rodenko et al. 1996; Mann et al. 2008). The MONET trial demonstrated that breast MRI was associated with an increased re-excision rate and is not advised to be used routinely for preoperative work-up of patients with non-palpable breast cancer (Peters et al. 2011). However, various authors proposed preoperative breast MRI to have significant impact in treatment of patients with ILC (Kim et al. 2011; Lopez & Bassett 2009; Michael et al. 2008; Qayyum et al. 2002; Mann et al. 2008; Boetes et al. 2004; Schelfout 2004). MRI has a superior accuracy (Berg et al. 2004; Boetes et al. 2004) in defining the extent of ILC and is, therefore, essential for a correct surgical planning and further treatment of these patients (Boetes et al. 1995; Orel et al. 1994; Rodenko et al. 1996; Mann et al. 2008; Peters et al. 2011; Lesser et al. 1982).
Invasive ductolobular carcinoma, also called invasive ductal carcinoma with lobular features (IDC-L), is intermediate in the histological spectrum from ILC to IDC, but the clinical and radiological presentation and behavior of this histological type have not been widely studied. It is therefore not well known if imaging features, clinicopathologic behavior, and outcome of these tumors are more comparable to IDC or to ILC.
The aim of this study was to therefore describe the spectrum of mammographic, sonographic and MRI features according to the BI-RADS® lexicon in patients with histologically proven invasive ductolobular carcinoma of the breast and to evaluate the relationship between the proportion of the lobular component and the imaging characteristics of these breast tumors.
Patients diagnosed with invasive breast carcinoma containing lobular features at the UMC Utrecht (The Netherlands) between January 2008 and October 2012 were considered. Only patients who underwent pre-operative MRI, mammography and US were included in this study.
For the mammograms, the standard craniocaudal view and mediolateral oblique were obtained using the Hologic Lorad Selenia full field digital mammography system. Additional views or spot compression were obtained when necessary. The US images were acquired using a Philips HD-11 XE digital imaging system (5–12 MHz linear probe).
The MRI scans were acquired with the patient in the prone position on 3 Tesla clinical MRI scanners (Achieva, Phillips Healthcare, Best, The Netherlands) equipped with dedicated phased-array bilateral breast coils (SENSE-Breast7TX and SENSE-Breast-4 MRI devices).
MRI imaging was performed according to our standard staging breast imaging protocol, which included a transverse high-resolution T1-weighted isotropic volume examination (THRIVE) [TE/TR 1.87/4.9 ms; flip angle 10°; FOV 360 × 360 × 180 mm3, acquired voxel size 0.65 × 0.65 × 2.0 mm3, reconstructed voxel size 0.64 × 0.64 × 1.00 mm3) and a transverse SPAIR T2-weighted series (TE/TR 100/5508 ms; inversion delay SPAIR 305 ms; flip angle 90°; FOV 360 × 360 × 180 mm3, acquired voxel size 1.00 · 1.46 · 2.0 mm3, reconstructed voxel size 0.64 · 0.64 · 2.00 mm3). The dynamic series consisted of contrast-enhanced fat-suppressed T1-weighted gradient echo images (TE/TR 1.24/3.3 ms; flip angle 10°; FOV 360 · 360 × 180 mm3, acquired voxel size 1.00 · 1.00 · 2.00 mm3, reconstructed voxel size 0.94 · 0.94 · 1.00 mm3; dynamic scan duration 68 seconds). Images were acquired before and at 0, 69, 138, 206, 274 and 342 seconds after the administration of 0.1 mmol/kg Gadolinium-DTPA (Magnevist, Schering, Germany). The acquisition time of this scan package was approximately 25 minutes.
Mammograms and US images were retrieved from the local PACS system and analyzed at a Sectra Workstation IDS7 (Sectra Imtec AB, Sweden). MRI examinations were processed by CADstream (Confirma, Inc., Kirkland, WA, USA). The images were interpreted by two dedicated breast radiologists. In addition, all images were reviewed and interpreted by a third radiologist, who was blinded to the proportion of the lobular component of each patient. In case of discordance with the original reports, a consensus was reached with a fourth dedicated breast radiologist with more than 20 years of experience in breast imaging.
All images were interpreted according to the guidelines of the BI-RADS® lexicon (D’Orsi & Dea 2003). Lesions were essentially divided into mass and non-mass-like lesions in order to perform morphological analysis. Based on the BI-RADS® lexicon, (D’Orsi & Dea 2003) lesions which had a mass as the main characteristic [isolated mass or dominant mass surrounded by smaller masses or foci of non-mass like enhancement (NMLE)] were defined as a mass-like lesion. Architectural distortion and NMLE (focal area, linear, ductal, segmental, regional, multiple regions, diffuse enhancement, and multiple enhancing foci) were defined as descriptors of non-mass-like lesion. Time intensity curves were classified according to their pattern of initial rise (slow, medium, rapid) and according to the delayed phase (persistent, plateau, washout). Finally, each lesion was scored according to the BI-RADS® lexicon; (D’Orsi & Dea 2003) 0 – Finding for which additional evaluation is needed, 1 – No abnormal enhancement, no lesion found, 2 – Benign finding, 3 – Probably benign finding, (short interval follow-up), 4 – Suspicious abnormality, 5 – Highly suggestive of malignancy, 6 – Known cancer biopsy-proven malignancy diagnosis on the imaged finding prior to definitive therapy.
Tumor extent and additional disease were defined as follows:
Multifocality: an additional malignant lesion in the same quadrant, separated from the index tumor by benign tissue.
Multicentricity: an additional malignant lesion in a different quadrant than the index cancer.
Contralateral disease: an additional malignant lesion found in contralateral breast.
Multiplicity: two or more of these features: multifocality, multicentricity and contralateral disease.
Additional findings were considered true positives when histopathological analysis of either preoperative work-up or surgical specimen has shown malignancy [invasive carcinoma or ductal carcinoma in situ (DCIS)].
All slices of ductolobular carcinoma (n = 113) were reviewed by a dedicated breast radiologist to quantify the lobular component, defined as a proportion of the invasive cancer.
Data were analysed using SPSS 17.0 software (SPSS, Inc., Chicago, IL, USA). Chi – square tests were used to compare proportions of the lobular component to the imaging characteristics and to compare the proportions of lobular component to the additional findings in our sample. For statistical purpose, proportion of the lobular component was grouped into three different categories: ≤ 20%, 21 – 94%, and ≥ 95%. Results were considered significant at p < 0.05.
Between January 2008 and October 2012, 505 patients were diagnosed with breast cancer and invasive ductal carcinoma with lobular features was reported in 30% (155/505) of the patients. Of these 155, 41 patients were excluded due to technical problems in performing MRI, obesity, claustrophobia, impossibility of obtaining mammography or ultrasound before MRI and personal reasons. The remaining 113 patients who underwent mammography, ultrasound and MRI were selected for this study. The age at diagnosis of the 113 patients ranged from 34 to 87 years with a mean of 57.4 years.
There were 41 patients with a proportion of ≤ 20% of lobular component, 36 patients with a proportion of 21 to 94%, and 36 patients with ≥ 95% of lobular component.
Mammographic findings of invasive ductolobular carcinomas of the breast
n = 113
Mass with calcification
Focal asymmetry or asymmetry
Asymmetry and calcification
n = 62
n = 62
n = 62
n = 113
Enlarged axillary lymph nodes
Imaging findings of invasive ductolobular carcinomas of the breast according to proportion of the lobular component
Proportion lobular component
21 – 94%
(n = 41)
(n = 36)
(n = 36)
Normal Mammographic Findings
The prevalence of other mammographic lesions (microcalcifications, architectural distortion, asymmetries), mass shape and mass margins did not vary significantly according to the proportion of the lobular component.
Ultrasonographic findings of invasive ductolobular carcinomas of the breast
n = 113
Other findings (parasternal mass)
n = 109
n = 109
n = 109
Mass Posterior acoustic feature
n = 109
n = 113
Enlarged axillary lymph nodes
Taking into account the lobular component, angular margins were more prevalent in patients with a bigger lobular component, with 11.1% in the ≥ 95% group and 4.8% in the ≤ 20% group. However, these results had no statistical significance. Findings concerning to mass shape, echogenicity and posterior acoustic features had similar prevalence in all groups.
MRI findings of invasive ductolobular carcinomas of the breast according to the BI-RADS® (NMLE = non-mass like enhancement)
n = 113
Mass + NMLE
Architectural distortion + NMLE
n = 101
High central low peripheric
n = 101
Low central high peripheric
n = 101
n = 101
n = 101
Dark internal septation
Enhancing internal septation
n = 45
NMLE Internal Enhancement
n = 45
n = 45
Kinetic Pattern Initial Rise
n = 113
Kinetic Pattern Delayed Phase
n = 113
39.8% of patients presented with NMLE features and they could be found isolated or associated with other lesions (adjacent to a dominant mass or to an architectural distortion). Considering all cases with NMLE features found in our sample (45 in total), 71.1% presented as focal areas. The internal enhancement was homogeneous in 69.0% and all cases were asymmetric.
Lesions with isolated NLME aspect were seen in 5.3% (6/113) of our patients. Architectural distortion and architectural distortion associated with NMLE were seen in 2.6% and 0.9% of the patients, respectively. Normal exams were found in 2 patients (1.8%).
We found 46 associated findings in 36 patients (31.8%), such as nipple retraction, skin thickening (focal or diffuse), edema, hematoma/blood and pre-contrast high ductal signal. Invasion of the pectoral muscle, confirmed by histopathological analysis, was found in 5 (4.4%) patients, nipple invasion in 3 (2.6%) patients and skin invasion in 2 (1.8%) cases. Chest wall invasion was seen in 1 (0.9%) patient, associated to pectoral muscle ingrowth and, in 2 (1.8%) cases, nipple, skin and pectoral muscle ingrowth were found together (Figures 2b, c, d, 3b and 5a).
Lymph node metastasis was histologically reported in 57 patients. From these, 38.5% were seen by imaging. In 5 cases, lymphadenopathy was seen both in MRI and US and in 3 cases it was seen in MRI, US and mammography. Prevalence of lymphadenopathy did not show significant differences according to proportion of the lobular component.
Multifocality and Multicentricity were found in 31 (27.4%) and 20 (17.7%) patients respectively. Multiplicity was found in 19 cases (16.8%) and contralateral disease was seen in 14 (12.3%) patients (Figure 2c and 4b). Taking into account the proportion of lobular component, contralateral disease, multifocality and multicentricity had higher prevalence rates in patients with bigger lobular component (Table 2), but there was no statistical significance. Nevertheless, multiplicity was more likely to be found in patients with a bigger lobular component (p = 0.021).
At mammography and US, tumor size ranged from 4 to 6.0 cm (mean, 1.78 cm) and on MRI tumor size ranged from 2 to 9.4 cm (mean, 2.50 cm). The sizes found on pathology ranged from 2 to 12.0 cm (mean, 2.9 cm).
The characteristics of IDC and ILC have been extensively described in literature. The dispersed infiltrating growth pattern of ILC with very little desmoplastic reaction and, consequently, the development of palpable lesion or tumors detectable in imaging exams, is less frequent. Normal or benign findings are more common in ILC than in IDC (8%–16% vs. 1.1%) (Li et al. 2003; Kim et al. 2011; Selinko et al. 2004; Mann et al. 2008) and false negative rates for ILC in mammography range from 14 to 19% (Kim et al. 2011; Hilleren et al. 1991b; Krecke & Gisvold 1993).
In the current study, we observed 15% (17/113) of normal or benign mammograms, which might demonstrate a similar behavior to ILC. It was also interesting that patients with tumors with ≥ 95% of lobular component had a higher prevalence of normal findings in mammography than patients with ≤ 20% of lobular component (25 vs. 12%, respectively), but these differences were not statistically significant.
ILC is usually seen as a mass (44%–65% of cases), (Lopez & Bassett 2009; Helvie et al. 1993) having predominantly irregular and spiculated margins (63-71%) (Helvie et al. 1993; Evans et al. 2002) and is usually isodense when compared to the fibroglandular tissue (Kim et al. 2011; Lopez & Bassett 2009; Sickles 1991). These numbers were similar to our present findings. Mass was found in 54.8% of our sample and 62.9% of these masses were simultaneously irregular, spiculated and isodense.
ILC spreading diffusely through the breast stroma leads to lower tendency to form round and circumscribed masses, only seen 1%–3% of cases of ILC (Le et al. 1992). The lobular component of ductolobular tumors might lead to a similar behavior and, in our study, circumscribed masses were indeed only found in 2.6% of our cases.
Architectural distortion was seen in 10.6% of cases and asymmetries were found in 7.9% of cases. Literature findings refers 10%–16% of ILC cases manifesting as architectural distortion (Hilleren et al. 1991b; Helvie et al. 1993) and 4%–13% of cases expressing as asymmetries (Hilleren et al. 1991b; Helvie et al. 1993). Our findings are comparable to these ILC mammographic lesions. However, architectural distortion is the second most common finding in ILC (Hilleren et al. 1991b;Helvie et al. 1993) and architectural distortion was the third most common radiological abnormality in our study.
It is well known that microcalcifications are much less common when comparing ILC and other breast carcinomas (4-24% vs. 41%) (Le et al. 1992). The prevalence of microcalcifications in our study was similar to the referred prevalence of these findings in ILC (11.5%).
US is considered more sensitive than mammography in detecting ILC. Literature reports sensitivities ranging from 68 to 98% (Paramagul et al. 1995; Selinko et al. 2004) and this imaging modality is also more accurate in identifying multifocality, multicentricity and size of the lesion (Selinko et al. 2004). According to Kim and Butler, mass has been described as being the most common lesion found in US in cases of ILC (60.5 – 100%) and both authors agreed that an irregular, hypoechoic mass, with spiculated margins and posterior acoustic shadowing is the most ordinary pattern seen in US images of ILC (Kim et al. 2011; Butler et al. 1999). Our results are consistent with these numbers. However, Kim et al. described US features of ILC and IDC as being very similar, except for posterior acoustic features, which has been described as being more related to ILC (Kim et al. 2011).
MRI has proven to have a high overall sensitivity (approximately 95%) (Mann et al. 2008; Kneeshaw 2003) and, in adjunct to mammography and US, has an essential importance in diagnostic and staging of ILC. MRI has a moderate specificity (67.4%) (Bluemke et al. 2004) and the routinely clinical use of this imaging modality might lead to unnecessary procedures (Peters et al. 2011). However, in ILC cases, MRI is superior to other imaging modalities in estimating tumor size, detecting multifocality, multicentricity, contralateral disease (Boetes et al. 1995; Orel et al. 1994; Rodenko et al. 1996; Mann et al. 2008; Peters et al. 2011; Lesser et al. 1982). and also affecting surgical management in 28% of cases (Mann et al. 2008; Weinstein 2001). Mass is considered the most common manifestation of ILC at MRI and the incidence varies substantially (45%–95%) (Kim et al. 2011; Rodenko et al. 1996; Schelfout 2004; Weinstein 2001; Yeh et al. 2003). Most of these studies have not described ILC findings in MRI strictly according to the BI-RADS® lexicon. However, Hye Na Jung and Kim found 92% and 88.8% of ILC cases presented as mass - like lesion according to the BI-RADS® (Kim et al. 2011; Jung et al. 2013). These findings are consistent with our research (89.4% of cases presenting as mass - like tumors).
In a literature review, Mann et all described 85.5% (65/76) of ILC tumors presenting as an irregular or spiculated mass (Mann et al. 2008). Our study had similar results and 91% (92/101) of the lesions were described as irregular or spiculated masses.
T1 and T2 features of lobular tumors are not frequently mentioned in literature. Levrini reported 95.2% (20/21) of cases of ILC tumors being hypo- and hyperintense lesions on T2 weighted TSE images (Levrini et al. 2008). Unfortunately all of our patients underwent diagnostic procedures within 10 days before MRI. The hemorrhage, edema and necrosis that result from these procedures may have changed T1 and/or T2 signal, which makes an accurate analysis more difficult.
Not many studies refer to the kinetic behavior of ILC. The infiltrative growth pattern of these tumors seems not to require extensive neovascularization and the lack of endothelial growth factor found in lobular tumors turns the new vessels to grow more slowly and having better maturation, resulting in less permeable capillaries (Lee et al. 1998). Some studies found ILC having delayed maximum enhancement and wash out pattern was not observed in the majority of tumors (Trecate et al. 2001; Sittek et al. 1998). These features might be due the histological behavior of ILC. Indeed, the prevalence of “plateau” curve in our study was higher in groups of patients with higher lobular component, and washout was more prevalent in groups of patients with lower lobular component. However, these differences were not statistically significant.
More recent studies refer 70.3% to 95.2% of ILC lesions having washout pattern (Kim et al. 2011; Levrini et al. 2008; Mann et al. 2011). Considering all available kinetic curves and not taking into account the proportion of the lobular component, washout was the most common pattern in our analysis (61.2%), but still lower than the numbers referred from these authors. However, Mann at al. showed that when CAD-application was used to evaluate the kinetic curve of lesions of ILC and IDC, washout pattern has a very similar prevalence in both tumors, which is not the case for visual assessment. In this latter case, IDC has a much higher prevalence of washout than ILC (Mann et al. 2011). The use of CADstream software to obtain the kinetic curves in our study might be the explanation for the higher washout pattern prevalence.
Arps et al. described IDC-L as having a higher frequency of nodal metastasis when compared to IDC and ILC (51 vs. 34 and 45%, respectively) (Arps et al. 2013). A similar result was seen in our study and lymph node metastasis was found in 50.4% of our sample (57/113), even though there was no statistical significance between prevalence of lymphadenopathy and proportions of lobular component.
Since comprehensive studies about mixed tumors are missing in literature, it is difficult to put our present results into perspective. Arps et al. compared clinicopathologic features and outcomes of 183 cases of IDC-L with lobular features with 1499 patients with IDC and 375 patients with ILC. The authors concluded that the clinicopathologic features and outcomes of IDC-L and ILC are very similar, irrespective of the proportion of the lobular component (Arps et al. 2013).
In our study, not only imaging characteristics did not vary significantly according to the lobular component, but also multifocality, multicentricity, contralateral disease and the proportions of lobular component did not show a statistically significant correlation.
However, the significant association between two or more of these additional findings (multiplicity) and bigger lobular component (p = 0.021) is in line with the higher rates of additional disease foci in patients with ILC (Boetes et al. 1995; Orel et al. 1994; Rodenko et al. 1996; Mann et al. 2008; Peters et al. 2011; Lesser et al. 1982).
To our knowledge, this is the first study to exclusively describe radiological features of invasive ductolobular carcinoma. They typically present as an irregular, spiculated and isodense mass at mammography, as a hypoechoic, irregular and spiculated mass with posterior acoustic shadowing on US, and as an isolated mass or as a dominant mass surrounded by smaller masses or NMLE on MRI. Washout is the most ordinary kinetic pattern of these tumors. Except for isodensity and multiplicity, the imaging characteristics did not vary significantly according to proportion of the lobular component. The imaging features and the high incidence of additional malignant imaging findings of invasive ductolobular carcinoma are therefore more similar to ILC than to IDC.
The study complies with current Dutch legislation.
- Acs G, Lawton TJ, Rebbeck TR, LiVolsi VA, Zhang PJ: Differential expression of E-cadherin in lobular and ductal neoplasms of the breast and its biologic and diagnostic implications. Am J Clin Pathol 2001, 115(1):85-98. 10.1309/FDHX-L92R-BATQ-2GE0View ArticleGoogle Scholar
- Arpino G, Bardou VJ, Clark GM, Elledge RM: Infiltrating lobular carcinoma of the breast: tumor characteristics and clinical outcome. Breast Cancer Res 2004, 6(3):R149-R156. 10.1186/bcr767View ArticleGoogle Scholar
- Arps DP, Healy P, Zhao L, Kleer CG, Pang JC: Invasive ductal carcinoma with lobular features: a comparison study to invasive ductal and invasive lobular carcinomas of the breast. Breast Cancer Res Treat 2013, 138(3):719-726. 10.1007/s10549-013-2493-2View ArticleGoogle Scholar
- Berg WA, Gutierrez L, NessAiver MS, Carter WB, Bhargavan M, Lewis RS, Ioffe OB: Diagnostic accuracy of mammography, clinical examination, US, and MR imaging in preoperative assessment of breast cancer. Radiology 2004, 233(3):830-849. 10.1148/radiol.2333031484View ArticleGoogle Scholar
- Biglia N, Mariani L, Sgro L, Mininanni P, Moggio G, Sismondi P: Increased incidence of lobular breast cancer in women treated with hormone replacement therapy: implications for diagnosis, surgical and medical treatment. Endocr Relat Cancer 2007, 14(3):549-567. 10.1677/ERC-06-0060View ArticleGoogle Scholar
- Biglia N, Maggiorotto F, Liberale V, Bounous VE, Sgro LG, Pecchio S, D’Alonzo M, Ponzone R: Clinical-pathologic features, long term-outcome and surgical treatment in a large series of patients with invasive lobular carcinoma (ILC) and invasive ductal carcinoma (IDC). Eur J Surg Oncol 2013, 39(5):455-460. 10.1016/j.ejso.2013.02.007View ArticleGoogle Scholar
- Bluemke DA, Gatsonis CA, Chen MH, et al.: Magnetic resonance imaging of the breast prior to biopsy. JAMA 2004, 292(22):2735-2742. 10.1001/jama.292.22.2735View ArticleGoogle Scholar
- Boetes C, Mus RD, Holland R, Barentsz JO, Strijk SP, Wobbes T, Hendriks JH, Ruys SH: Breast tumors: comparative accuracy of MR imaging relative to mammography and US for demonstrating extent. Radiology 1995, 197(3):743-747.View ArticleGoogle Scholar
- Boetes C, Strijk SP, Holland R, Barentsz JO, Van Der Sluis RF, Ruijs JH: False-negative MR imaging of malignant breast tumors. Eur Radiol 1997, 7(8):1231-1234. 10.1007/s003300050281View ArticleGoogle Scholar
- Boetes C, Veltman J, van DL, Bult P, Wobbes T, Barentsz JO: The role of MRI in invasive lobular carcinoma. Breast Cancer Res Treat 2004, 86(1):31-37. 10.1023/B:BREA.0000032921.10481.dcView ArticleGoogle Scholar
- Brem RF, Ioffe M, Rapelyea JA, Yost KG, Weigert JM, Bertrand ML, Stern LH: Invasive lobular carcinoma: detection with mammography, sonography, MRI, and breast-specific gamma imaging. AJR Am J Roentgenol 2009, 192(2):379-383. 10.2214/AJR.07.3827View ArticleGoogle Scholar
- Butler RS, Venta LA, Wiley EL, Ellis RL, Dempsey PJ, Rubin E: Sonographic evaluation of infiltrating lobular carcinoma. AJR Am J Roentgenol 1999, 172(2):325-330. 10.2214/ajr.172.2.9930776View ArticleGoogle Scholar
- Chapellier C, Balu-Maestro C, Bleuse A, Ettore F, Bruneton JN: Ultrasonography of invasive lobular carcinoma of the breast: sonographic patterns and diagnostic value: report of 102 cases. Clin Imaging 2000, 24(6):333-336. 10.1016/S0899-7071(00)00234-5View ArticleGoogle Scholar
- D’Orsi CJ, Dea MEI: Breast Imaging Reporting and Data System: ACR BI-RADS - Breast Imaging Atlas. Reston,VA: American College of Radiology; 2003.Google Scholar
- Evans WP, Warren Burhenne LJ, Laurie L, O’Shaughnessy KF, Castellino RA: Invasive lobular carcinoma of the breast: mammographic characteristics and computer-aided detection. Radiology 2002, 225(1):182-189. 10.1148/radiol.2251011029View ArticleGoogle Scholar
- Framarino Dei MM, Fiorelli C, Bandiera AF, Veneziano M, Galati GM, Porfiri L: Infiltrating lobular carcinoma of the breast (ILC). Diagnostic and therapeutic aspects. Eur J Gynaecol Oncol 1995, 16(1):36-39.Google Scholar
- Harms SE, Flamig DP, Hesley KL, Meiches MD, Jensen RA, Evans WP, Savino DA, Wells RV: MR imaging of the breast with rotating delivery of excitation off resonance: clinical experience with pathologic correlation. Radiology 1993, 187(2):493-501.View ArticleGoogle Scholar
- Helvie MA, Paramagul C, Oberman HA, Adler DD: Invasive lobular carcinoma. Imaging features and clinical detection. Invest Radiol 1993, 28(3):202-207. 10.1097/00004424-199303000-00002View ArticleGoogle Scholar
- Hilleren DJ, Andersson IT, Lindholm K, Linnell FS: Invasive lobular carcinoma: mammographic findings in a 10-year experience. Radiology 1991a, 178(1):149-154.View ArticleGoogle Scholar
- Hilleren DJ, Andersson IT, Lindholm K, Linnell FS: Invasive lobular carcinoma: mammographic findings in a 10-year experience. Radiology 1991b, 178(1):149-154.View ArticleGoogle Scholar
- Jung HN, Shin JH, Han BK, Ko EY, Cho EY: Are the imaging features of the pleomorphic variant of invasive lobular carcinoma different from classic ILC of the breast? Breast 2013, 22(3):324-329. 10.1016/j.breast.2012.07.016View ArticleGoogle Scholar
- Kim SH, Cha ES, Park CS, Kang BJ, Whang IY, Lee AW, Song BJ, Park J: Imaging features of invasive lobular carcinoma: comparison with invasive ductal carcinoma. Jpn J Radiol 2011, 29(7):475-482. 10.1007/s11604-011-0584-8View ArticleGoogle Scholar
- Kneeshaw PJ: Dynamic contrast enhanced magnetic resonance imaging aids the surgical management of invasive lobular breast cancer. Eur J Oncol 2003, 29(1):32-37. 10.1053/ejso.2002.1391View ArticleGoogle Scholar
- Korhonen T, Huhtala H, Holli K: A comparison of the biological and clinical features of invasive lobular and ductal carcinomas of the breast. Breast Cancer Res Treat 2004, 85(1):23-29. 10.1023/B:BREA.0000021038.97593.8bView ArticleGoogle Scholar
- Krecke KN, Gisvold JJ: Invasive lobular carcinoma of the breast: mammographic findings and extent of disease at diagnosis in 184 patients. AJR Am J Roentgenol 1993, 161(5):957-960. 10.2214/ajr.161.5.8273634View ArticleGoogle Scholar
- Le GM, Ollivier L, Asselain B, Meunier M, Laurent M, Vielh P, Neuenschwander S: Mammographic features of 455 invasive lobular carcinomas. Radiology 1992, 185(3):705-708.View ArticleGoogle Scholar
- Lee AH, Dublin EA, Bobrow LG, Poulsom R: Invasive lobular and invasive ductal carcinoma of the breast show distinct patterns of vascular endothelial growth factor expression and angiogenesis. J Pathol 1998, 185(4):394-401. 10.1002/(SICI)1096-9896(199808)185:4<394::AID-PATH117>3.0.CO;2-SView ArticleGoogle Scholar
- Lesser ML, Rosen PP, Kinne DW: Multicentricity and bilaterality in invasive breast carcinoma. Surgery 1982, 91(2):234-240.Google Scholar
- Levrini G, Mori CA, Vacondio R, Borasi G, Nicoli F: MRI patterns of invasive lobular cancer: T1 and T2 features. Radiol Med 2008, 113(8):1110-1125. 10.1007/s11547-008-0308-zView ArticleGoogle Scholar
- Li CI, Anderson BO, Daling JR, Moe RE: Trends in incidence rates of invasive lobular and ductal breast carcinoma. JAMA 2003, 289(11):1421-1424. 10.1001/jama.289.11.1421View ArticleGoogle Scholar
- Lopez JK, Bassett LW: Invasive lobular carcinoma of the breast: spectrum of mammographic, US, and MR imaging findings. Radiographics 2009, 29(1):165-176. 10.1148/rg.291085100View ArticleGoogle Scholar
- Mann RM, Hoogeveen YL, Blickman JG, Boetes C: MRI compared to conventional diagnostic work-up in the detection and evaluation of invasive lobular carcinoma of the breast: a review of existing literature. Breast Cancer Res Treat 2008, 107(1):1-14.View ArticleGoogle Scholar
- Mann RM, Veltman J, Huisman H, Boetes C: Comparison of enhancement characteristics between invasive lobular carcinoma and invasive ductal carcinoma. J Magn Reson Imaging 2011, 34(2):293-300. 10.1002/jmri.22632View ArticleGoogle Scholar
- Michael M, Garzoli E, Reiner CS: Mammography, sonography and MRI for detection and characterization of invasive lobular carcinoma of the breast. Breast Dis 2008, 30: 21-30.Google Scholar
- Moran MS, Yang Q, Haffty BG: The Yale University experience of early-stage invasive lobular carcinoma (ILC) and invasive ductal carcinoma (IDC) treated with breast conservation treatment (BCT): analysis of clinical-pathologic features, long-term outcomes, and molecular expression of COX-2, Bcl-2, and p53 as a function of histology. Breast J 2009, 15(6):571-578. 10.1111/j.1524-4741.2009.00833.xView ArticleGoogle Scholar
- Mumtaz H, Hall-Craggs MA, Davidson T, Walmsley K, Thurell W, Kissin MW, Taylor I: Staging of symptomatic primary breast cancer with MR imaging. AJR Am J Roentgenol 1997, 169(2):417-424. 10.2214/ajr.169.2.9242745View ArticleGoogle Scholar
- Orel SG, Schnall MD: MR imaging of the breast for the detection, diagnosis, and staging of breast cancer. Radiology 2001, 220(1):13-30. 10.1148/radiology.220.1.r01jl3113View ArticleGoogle Scholar
- Orel SG, Schnall MD, LiVolsi VA, Troupin RH: Suspicious breast lesions: MR imaging with radiologic-pathologic correlation. Radiology 1994, 190(2):485-493.View ArticleGoogle Scholar
- Paramagul CP, Helvie MA, Adler DD: Invasive lobular carcinoma: sonographic appearance and role of sonography in improving diagnostic sensitivity. Radiology 1995, 195(1):231-234.View ArticleGoogle Scholar
- Peters NH, Borel Rinkes IH, Zuithoff NP, Mali WP, Moons KG, Peeters PH: Meta-analysis of MR imaging in the diagnosis of breast lesions. Radiology 2008, 246(1):116-124. 10.1148/radiol.2461061298View ArticleGoogle Scholar
- Peters NH, van ES, van den Bosch MA, et al.: Preoperative MRI and surgical management in patients with nonpalpable breast cancer: the MO. Eur J Cancer 2011, 47(6):879-886. 10.1016/j.ejca.2010.11.035View ArticleGoogle Scholar
- Qayyum A, Birdwell RL, Daniel BL, Nowels KW, Jeffrey SS, Agoston TA, Herfkens RJ: MR imaging features of infiltrating lobular carcinoma of the breast: histopathologic correlation. AJR Am J Roentgenol 2002, 178(5):1227-1232. 10.2214/ajr.178.5.1781227View ArticleGoogle Scholar
- Qureshi HS, Linden MD, Divine G, Raju UB: E-cadherin status in breast cancer correlates with histologic type but does not correlate with established prognostic parameters. Am J Clin Pathol 2006, 125(3):377-385.View ArticleGoogle Scholar
- Rodenko GN, Harms SE, Pruneda JM, Farrell RS Jr, Evans WP, Copit DS, Krakos PA, Flamig DP: MR imaging in the management before surgery of lobular carcinoma of the breast: correlation with pathology. AJR Am J Roentgenol 1996, 167(6):1415-1419. 10.2214/ajr.167.6.8956569View ArticleGoogle Scholar
- Sastre-Garau X, Jouve M, Asselain B, Vincent-Salomon A, Beuzeboc P, Dorval T, Durand JC, Fourquet A, Pouillart P: Infiltrating lobular carcinoma of the breast. Clinicopathologic analysis of 975 cases with reference to data on conservative therapy and metastatic patterns. Cancer 1996, 77(1):113-120. 10.1002/(SICI)1097-0142(19960101)77:1<113::AID-CNCR19>3.0.CO;2-8View ArticleGoogle Scholar
- Schelfout K: Preoperative breast MRI in patients with invasive lobular breast cancer. Eur Radiol 2004, 14(7):1209-1216.View ArticleGoogle Scholar
- Selinko VL, Middleton LP, Dempsey PJ: Role of sonography in diagnosing and staging invasive lobular carcinoma. J Clin Ultrasound 2004, 32(7):323-332. 10.1002/jcu.20052View ArticleGoogle Scholar
- Sickles EA: The subtle and atypical mammographic features of invasive lobular carcinoma. Radiology 1991, 178(1):25-26.View ArticleGoogle Scholar
- Sittek H, Perlet C, Untch M, Kessler M, Reiser M: Dynamic MR-mammography in invasive lobular breast cancer. Rontgenpraxis 1998, 51(7):235-242.Google Scholar
- Trecate G, Tess JD, Vergnaghi D, Bergonzi S, Mariani G, Ferraris C, Musumeci R: Lobular breast cancer: how useful is breast magnetic resonance imaging? Tumori 2001, 87(4):232-238.Google Scholar
- Verkooijen HM, Fioretta G, Vlastos G, et al.: Important increase of invasive lobular breast cancer incidence in Geneva, Switzerland. Int J Cancer 2003, 104(6):778-781. 10.1002/ijc.11032View ArticleGoogle Scholar
- Weinstein SP: MR imaging of the breast in patients with invasive lobular carcinoma. AJR Am J Roentgenol 2001, 176(2):399-406. 10.2214/ajr.176.2.1760399View ArticleGoogle Scholar
- Winston CB, Hadar O, Teitcher JB, Caravelli JF, Sklarin NT, Panicek DM, Liberman L: Metastatic lobular carcinoma of the breast: patterns of spread in the chest, abdomen, and pelvis on CT. AJR Am J Roentgenol 2000, 175(3):795-800. 10.2214/ajr.175.3.1750795View ArticleGoogle Scholar
- Yang WT, Hennessy B, Broglio K, Mills C, Sneige N, Davis WG, Valero V, Hunt KK, Gilcrease MZ: Imaging differences in metaplastic and invasive ductal carcinomas of the breast. AJR Am J Roentgenol 2007, 189(6):1288-1293. 10.2214/AJR.07.2056View ArticleGoogle Scholar
- Yeatman TJ, Cantor AB, Smith TJ, Smith SK, Reintgen DS, Miller MS, Ku NN, Baekey PA, Cox CE: Tumor biology of infiltrating lobular carcinoma. Implications for management. Ann Surg 1995, 222(4):549-559.View ArticleGoogle Scholar
- Yeh ED, Slanetz PJ, Edmister WB, Talele A, Monticciolo D, Kopans DB: Invasive lobular carcinoma: spectrum of enhancement and morphology on magnetic resonance imaging. Breast J 2003, 9(1):13-18. 10.1046/j.1524-4741.2003.09104.xView ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.