Enhancing patterns of breast cancer on preoperative dynamic contrast-enhanced magnetic resonance imaging and resection margin in breast conserving therapy

Abstract

BACKGROUND:

The association between enhancing patterns of preoperative dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) and resection margins after BCS has not been studied in detail before.

OBJECTIVE:

We investigated the association between surgical outcomes and enhancing patterns observed on DCE-MRI.

METHODS:

269 enhancing patterns on DCE-MRI scans were selected, and subdivided into the following groups: (1) a single mass-like enhancement, (2) a single non-mass-like enhancement (NME), (3) mass-like enhancing breast cancer with other mass-like enhancing lesions, and (4) mass-like enhancing breast cancer with additional NMEs. Associations between enhancing patterns on DCE-MRI and re-excision rate, size of specimen, and ratio of tumor/specimen were evaluated retrospectively.

RESULTS:

The conversion rate from breast conserving therapy (BCT) to mastectomy as a result of MRI findings was 13.4%, re-excision rate during BCT was 8.2% and excision rate of another suspicious lesion was 7.4%. The single NME group had the highest re-excision rate after BCT (22.2%) (p = 0.02). The ratio of tumor/specimen (p = 0.61) and mean specimen size (p = 0.38) were not influenced by enhancement patterns. The false positive rate and positive predictive values of using DCE-MRI for defining the extension of breast cancer was 22.2% and 71.4%, respectively.

CONCLUSION:

Enhancement patterns on DCE- MRI, especially NME, could increase re-excision rates.

Keywords

Breast neoplasm magnetic resonance imaging (MRI)non-mass-like enhancement mass breast conserving therapy re-excision

Abbreviations

DCE-MRI: Dynamic Contrast-Enhanced Magnetic Resonance Imaging,

NME: Non-Mass-like Enhancement,

IDC: Invasive Ductal Carcinoma,

EIC: Extensive Intraductal Component,

BCT: Breast Conserving Therapy

Introduction

A positive margin is defined as the presence of invasive ductal carcinoma or ductal carcinoma in situ (DCIS) at the inked surface of a breast cancer surgical specimen. It implies a potentially incomplete resection that is associated with a considerably higher risk of ipsilateral breast tumor recurrence (IBTR) [1–3]. Advocates of using MRI for diagnosis presume that the greater sensitivity for detecting cancer achieved with MRI will improve the patient selection process for BCT and increase the likelihood of obtaining negative margins at the first lumpectomy attempt. Several investigators have postulated that preoperative MRI would lead to a decrease in the rate of margin-positive partial mastectomy for breast cancer, although this has not been fully investigated [4,5]. Although some authors have recommended that breast MRI be used in patient selection for BCT [6–8], there is surprisingly little data to support this assertion and historic treatment data appear to contradict the need for routine breast MRI.

Three types of contrast-enhancing lesions on DCE-MRI are described by the Breast Imaging Reporting and Data Systems (BI-RADS) classification [9]: (1) a mass; (2) a non-mass enhancement (NME); or (3) a focus. The prevalence of NME in high-risk patients is significantly lower than that of mass lesions (13% versus 76%, respectively) [10,11]. It has been found that 57% of non-palpable invasive carcinomas may present as NME [12]. NME lesions have also been reported with non-invasive ductal carcinomas, lobular carcinomas in situ, atypical ductal hyperplasia, papillomas, hormonal changes, and fibrocystic disease [13,14].

The goals of this study were to analyze the relationship of contrast-enhancing lesions on DCE-MRI as currently used in our clinical practice without MRI- guided biopsy with short-term surgical outcomes, including rates of re-excision for positive resection margin during BCT, a conversion from attempted BCT to mastectomy, and addition of other surgical excisions.

Methods

Patient selection

In total, 304 consecutive women with primary operable breast cancer who were scheduled for breast conserving operations based on conventional imaging and palpation, and presenting at our hospital, were included between March 2010 and December 2012. Women receiving chemotherapy prior to surgery (n = 15), those with bilateral breast cancer (n = 1), and with local excisional biopsy (n = 19) were excluded. In total, 269 women with breast cancer confirmed histopathologically were enrolled. This study was approved by our institution’s Ethics and Investigation Committee (Heapaik-2012110).

MRI technique

MRI examinations were performed using a 1.5 T system (HDxt, GE Healthcare, Milwaukee WI, USA) or a 3.0 T system (Achieva 3.0T Tx; Philips Healthcare, Best, the Netherlands) with a dedicated surface breast coil (8-channel breast array coil, GE Medical Systems; 7-channel SENSE breast coil, Philips Medical Systems). Each patient was randomly assigned to one of the MRI systems according to the MRI suite schedule. The baseline MRI examination for both systems consisted of a fast spin-echo T1-weighted and a short T1-inversion recovery or spectral presaturation attenuated inversion recovery (SPAIR) T2-weighted sequence, a SPAIR single-shot echo-planar imaging diffusion-weighted sequence, and a three-dimensional dynamic contrast-enhanced sequence. Before contrast agent injection, diffusion-weighted images were obtained for both breasts in the axial plane with the diffusion gradient applied in the orthogonal direction (bipolar gradient scheme; bandwidth 250 Hz on the 1.5 T system and 32.4 Hz on the 3.0 T system). Diffusion-weighted images were performed withb -values of 0 and 1000 s/mm² . DCE-MRI examinations were obtained in the axial plane. One pre- and five post-contrast dynamic series were acquired every 77 seconds on the 1.5 T system and every 60 seconds on the 3.0 T system after bolus injection of 0.5 mmol/L of gadoterate meglumine (Dotarem, Guerbet, Aulnay-sous-Bois, France) per kilogram of body weight into an antecubital vein. The injection rate was 2 mL/second, followed by a 20-mL saline flush. Standard subtraction images were obtained by subtracting the pre-contrast images from the early peak post-contrast images on a pixel-by-pixel basis. Reverse subtraction images were generated by subtracting the last post-contrast image from the early peak post-contrast image. Maximum intensity projection images were reconstructed using the subtraction images.

Interpretation of enhancing lesions in DCE-MRI

Two radiologists (JHK, KSJ) each with 10 years of experience in breast MRI interpretations that were unaware of the pathological and immunochemical findings independently assessed the images. Breast MRIs were interpreted according to the American College of Radiology breast imaging reporting and data system (ACR BIRADS) MRI lexicon. We divided all lesions into two categories such as mass including foci and NME. A focus is a tiny spot of enhancement smaller than 0.5 cm in diameter and a mass is a three-dimensional space-occupying lesion larger than 0.5 cm in diameter. NME is enhancement of an area that is not a mass [9]. If a lesion had a speculative appearance, it was regarded as a morphologically suspicious lesion. Additional lesions were identified in some breasts separate from biopsy-proven breast cancers.

If additional suspicious lesions were visible on follow-up ultrasound, the patient underwent a core biopsy or surgical excision. In these patients, if these lesions were not visible on ultrasound, we performed a follow-up examination because our institution does not routinely use MR-guided biopsy. There were 86 patients (86∕269, 31.9%) who had additional suspicious lesions detected on DCE-MRI, and received a follow-up ultrasound. For these patients, differences in tumor diameter between ultrasound and DCE-MRI were evaluated and if it was more than 10 mm [15], it was considered as a discrepancy and predictive of the extension of breast cancer.

Histopathologic and immunohistochemical analysis

The histologic samples were stained with hematoxylin and eosin. The histologic grade of IDCs was determined using the modified Bloom and Richardson criteria [16]. Tumors were staged according to the TNM system [17], and the results were used for pathological staging. Estrogen (ER) and progesterone (PR) expression were recorded as either negative or positive. Her-2/neu (HER2) status was evaluated with an immunocytochemical assay (IHC) (Dako HercepTest, Dako Corp, CA, USA). IHC staining was semi-quantitatively evaluated using the American Society of Clinical Oncology/College of American Pathologists (ASCO/CAP) guidelines [18]. Staining results were scored as 0 (negative; no staining), 1 (negative; faint/barely perceptible incomplete membrane staining), 2 (equivocal; weak to moderate complete membrane staining in >10% of the tumor cells or strong, complete membrane staining in <30% of the tumor cells), and 3 (positive; strong complete membrane staining in >30% of the tumor cells). When the staining results were 2, Her-2/neu SISH was performed in a manner using the ASCO/CAP guidelines.

The cutoff point of Ki-67 positivity was 14%. A tumor was considered to have an extensive intraductal component (EIC) when ductal carcinoma in situ occupied 30% or more of the area encompassed by the infiltrating tumor and ductal carcinoma in situ was present in grossly normal adjacent breast tissue or clearly extended beyond the infiltrating edge of the tumor [19].

Breast cancer samples were categorized into breast cancer subtypes based on the IHC ER, PR, HER2, and Ki-67 status as surrogate definitions of intrinsic subtypes of breast cancer [20]. Luminal A tumors were ER+ and PR+, HER2-, and Ki-67 < 14%. Luminal B tumors were (1) luminal B-like (HER2-), ER+ and HER2-, and at least one with ‘high’ Ki-67%’, PR- or low; or (2) luminal B-like (HER2+); ER+, HER2 over-expressed or amplified, no K-67 expression, no PR. HER2 over-expressing tumors were ER-, PR-, and HER2+. Basal-like tumors were ER-, PR-, and HER2-.

Evaluation of resection margin

Intraoperative margin excision and frozen section analysis were performed for intraoperative margin evaluation in all patients using a perpendicular method. Breast tissue contains a large amount of fat, which creates particular difficulties when performing cryosection. The presence of atypical ductal/lobular hyperplasia (ADH/ALH), ductal carcinoma in situ (DCIS), or invasive ductal carcinomas (IDC) at the margins of excised breast tissues for invasive breast cancers was considered as evidence of positive surgical margin.

Patient review and definitions

We categorized 269 patients into four groups according to patterns of enhancing lesions on DCE-MRI. These groups included: (1) a single mass-like enhancement, (2) a single non-mass enhancement (NME) (Fig. 1), (3) mass-like enhancing breast cancer with other mass-like enhancing lesions, and (4) mass-like enhancing breast cancer with additional NMEs. We considered the following events as short term surgical outcomes; (1) the rate of re-excision for positive resection margin during BCT, (2) the rate of conversion from attempted BCT to mastectomy, and (3) the rate of additional surgical excisions.

Statistical analysis

A chi-squared test was used to explore the correlation between patterns of MRI-enhancing lesions and clinicopathological factors. The student’s t -test was performed for continuous normally distributed variables. Multiple linear regression analysis was used to determine which factors were the most influential in predicting enhancement patterns. A p -value <.05 was considered statistically significant. SAS software (version 9.1, SAS institute, NC, USA) was used to perform statistical analyses.

Results

Patient characteristics

At baseline, the study population contained 269 patients with breast cancer. The mean tumor diameter was 1.93 ± 1.31 cm. Of the total, 142 (52.8%) patients were staged as 0 or I, and 127 (47.2%) patients were stage II or III. The final operation method for 224 (83.2%) patients was breast conservation, and 45 modified radical mastectomy (17.8%). 81 (30.1%) patients had axillary lymph node metastases. 48 (16.7%) patients were classified with Luminal A, 91 (33.8%) with Luminal B (HER2-), 25 (9.3%) with Luminal B (HER2+), 55 (20.4%) had HER2 breast cancers, and 50 (18.6%) patients had basal-like breast cancers.

Correlation between pattern of enhancing lesions and clinicopathological parameters

Among 269 patients, 136 (50.6%) patients had a single breast cancer with a mass-like enhancing lesion, 47(17.5%) patients had a single breast cancer with NME in DCE-MRI, and 40 (14.9%) patients had a mass-like breast cancer with other mass-like enhancing lesions, and 46 (17.1%) patients had mass-like breast cancer with other NME lesions. Age (p = 0.04), operation method (p = 0.002), histologic type (p < 0.001), Ki-67 (p = 0.02), and EIC (p = 0.01) were significantly correlated with pattern of enhancing lesions (Table 1).

Multiple linear regression analysis of clinicopathologic features on pattern of enhancing lesions on DCE-MRI

Histologic type was most significantly correlated with pattern of enhancing lesions on DCE-MRI (p < 0.001), EIC positivity was also correlated with patterns of enhancing lesions on DCE-MRI (p = 0.05). However, age, and cancer stage were not correlated with pattern of enhancing lesions (Table 2).

Effects of enhancing lesions in DCE-MRI on breast cancer operation

MRI led to a change in multimodality treatment planning in 78 patients (28.9%). The conversion rate from BCT to mastectomy as a result of MRI finding was 13.4% (36∕269), re-excision rate during BCT was 8.2% (22∕269), and excision rate of another additional suspicious lesion was 7.4% (20∕269) (Table 3). 7 patients had atypical ductal hyperplasia or lobular carcinoma in situ in a resection margin, and 4 patients underwent re-excision (1.5%). Patients with single mass-like enhancing breast cancers had a lower rate of re-excision and mastectomy. However, single NME breast cancers or mass-like enhancing breast cancers with another NME had a higher rate of mastectomy or re-excision (p = 0.04) (Table 3). The ratio of tumor/specimen (p = 0.61), and mean of specimen size (p = 0.38) were not influenced by patterns of enhancing lesions (Table 3).

Within the 224 patients who underwent BCT, those with single NME breast cancers had a higher rate of re-excision, and those with mass-like enhancing breast cancers with a suspicious mass lesion had a higher rate of another excision or biopsy (p = 0.02) (Table 4). The ratio of tumor/specimen (p = 0.59), and mean of specimen size (p = 0.24) were not influenced by patterns of enhancing lesions (Table 4). In total, 36 patients underwent conversion from BCT to mastectomy with a false positive rate of 22.2%.The positive and negative predictive values on DCE-MRI regarding the definition of the extension of breast cancer were 71.4% and 50%, respectively (Table 5).

Discussion

Multiple studies have demonstrated that breast MRI detects foci of cancer not seen with other imaging modalities in 10%–30% of patients [21,22]. The American College of Radiology guidelines suggest that contrast-enhanced MRI of the breast may be useful to determine both the extent of disease and the presence of multifocality and multicentricity in patients with invasive carcinoma and DCIS. This has resulted in an enthusiastic adoption in women with newly diagnosed breast cancer. However, the rate of cancer detection with MRI significantly exceeds the risk of local recurrence in women selected for BCT without the use of MRI [23,24]. Further, BCT and mastectomy have been shown to produce equivalent treatment outcomes for long-term survival, long before the use of breast MRI [25].

Studies examining changes in surgical therapy because of MRI findings have shown a conversion from BCT to mastectomy in 6.5%–25% of patients, and performing a wide excision in an additional 3%–13.5% of patients [26–29]. In a recent meta-analysis of 19 studies that included 2763 patients undergoing pretreatment MRI, additional disease was found in 16%. Changes in surgical plan because of cancer in the areas of MRI abnormalities occurred in 11.3% [23,30]. Currently there is no convincing evidence that preoperative MRI improves surgical outcomes, such as the rate of positive margins, re-excision or breast conservation, in the average patients with breast cancer [31–33]. Vos et al. suggested that re-excision rates were 9.8% in the MRI group, with no difference in the non-MRI group (7.2%) Further, Vos et al indicated found that preoperative MRI did not influence the risk of margin involvement or re-excision rate after BCS, and that MRI scans should be more targeted and the general wide spread use be discouraged by a large, multicenter, population-based analysis [34]. Contradictionary results have been found in multiple small, single-centre studies that have focused on the surgical outcomes of BCS in patient with invasive breast cancer [35,36], and DCIS [37,38]. To date, only the MONET (MR mammography of Nonpalpable Breast Tumors) trial has focused on patients with non-palpable invasive cancer, and found that the addition of preoperative MRI to routine clinical care was associated with an increased re-excision rate [39].

The relationship between clinicopathologic parameters and contrast-enhancing pattern of breast cancers on DCE-MRI has been investigated, but the results are discrepant [40,41]. Enhancing patterns of breast cancers in preoperative MRI may result in a decrease in the rate of margin-positive BCT, however this has not been well-studied previously. Lee et al. [42] showed that morphologic type (mass versus NME) was not significantly associated with clinicopathologic factors (tumor size, lymph node status, and histological grade) or IHC prognostic factors (ER, PR, p53, HER2, Ki-67). Chen et al. [43] showed that ER-negative lesions were more likely to exhibit NME compared with ER-positive cancer. Compared with mass lesions, we found that NME was more commonly related to DCIS, similar to the findings of many previous studies [44,45]. We also found that the pattern of enhancing type, presence of suspicious multifocal or multicentric enhancing lesion was associated with a higher rate of margin positivity and higher rate of conversion from BCT to mastectomy. The re-excision rate (8.2%) compares very favorably with the most recently reported data (20%) [46]. However, the association between enhancing patterns of preoperative DCE-MRI and resection margins after BCS has not been studied in detail before.

Follow-up ultrasonography or MRI-guided core biopsy have been validated and should be used for accurate preoperative or intraoperative assessment for breast cancer size and extent [28,47]. Follow-up ultrasonography or MRI-guided core biopsy should minimize overtreatment and dose without substantially prolonging the time to initiation of definitive treatment [8]. The results of this work are significant when compared with other studies. Preoperative MRI identified suspicious multicentric or multifocal ipsilateral breast cancers in 31% of patients in this study. These patients were thought to be candidates for BCT with conventional imaging and clinical evaluation in agreement with [48,49] or greater than [8] published findings likely derived from improved local staging of tumor extent. This resulted in better selection of patients for BCT through follow-up ultrasonography or ultrasonography-guided biopsy or excision without MRI-guide biopsy. This study found that suspicious multifocal or multicentric lesions, which were detected and evaluated in preoperative DCE-MRI provided clinically meaningful information because of its association with re-excision during BCT and final mastectomy. Even though single breast cancers with NME had high rates of re-excision and final mastectomy rate, the ratio of tumor/specimen and mean of specimen size were not influenced by patterns of enhancing lesions. Further these patterns of enhancement did not influence surgeon decisions to make wider excisions.

This study has several limitations. The study population was not large enough to sufficiently evaluate the association between a change in operation method and enhancing types of MRI lesions. There was potential bias owing to the exclusion of many patients who were referred from other institutions with excisional biopsy, previous systemic therapy, or multiple suspicious lesions in DCE-MRI because we were unable to perform MRI-guided biopsy. Detailed correlations between histopathologic factors, such as microvessel density, structural vascular abnormalities, and kinetic characteristics were not performed. The retrospective, non-randomized design of the study also explains the differences in tumor characteristics, such as patients having extended DCIS component and being more likely to have a DCIS adjacent to invasive tumor could be particularly enrolled in a group with a single NME typed breast cancer. It is known that these factors increase the risk of incomplete excision, and this could be a confounding bias. In conclusion, this study found suspicious multifocal or multicentric lesions, but their enhancing patterns were associated with re-excision during BCT or mastectomy rate. Even though many patients had solitary lesions, single breast cancers with NME had a higher rate of re-excision or mastectomy. Owing to lack of evidence of the benefits of preoperative MRI regarding short- and long-term treatment outcomes, the value of preoperative MRI has been heavily dabated. But both histologic types and patterns of enhancing types in preoperative breast DCE-MRI might be considered in the decision regarding extent of resection during BCT.

Footnotes

Acknowledgements

JSL have made substantial contributions in the design of the study, acquiring the data, and drafting the initial manuscript. SJK and HKJ have made substantial contributions in evaluating the MR images. JSL have participated in drafting the article and SJK and OHK have approved the final submitted or revised version critically for important intellectual content and have given final approval of the version to be published.

Conflict of interest

The author(s) have no conflicts of interest to declare.

References

Houssami

, Macaskill

, Marinovich

, Meta-analysis of the impact of surgical margins on local recurrence in women with early stage invasive breast cancer treated with breast-conserving therapy, Eur J Cancer, 46: 3219–3232, 2010.

Azu

, Abrahamse

, Katz

, What is an adequate margin for breast conserving surgery? Surgeon attitudes and correlates, Ann Surg Oncol, 17: 558–563, 2010.

Taghian

, Mohiuddin

, Jagi

, Current perceptions regarding surgical margin status after breast conserving surgery: results of a survey, Ann Surg, 241: 629–639, 2005.

Henry-Tillman

, Harms

, Westbrook

, Role of breast magnetic resonance imaging in determining breast as a source of unknown metastatic lymphadenopathy, Am J Surg, 178: 496–500, 1999.

Schnall

, MR imaging evaluation of cancer extent: is there clinical relevance?, Magn Reson Imaging Clin N Am, 14: 379–381, 2006, vii.

Hollingsworth

, Stough

, O’Dell

, Brekke

, Breast magnetic resonance imaging for preoperative locoregional staging, Am J Surg, 196: 389–397, 2008.

Lalonde

, David

, Trop

, Magnetic resonance imaging of the breast: current indications, Can Assoc Radiol J, 56: 301–308, 2005.

Grobmyer

, Mortellaro

, Marshall

, Is there a role for routine use of MRI in selection of patients for breast-conserving cancer therapy?, J Am Coll Surg, 206: 1042–1050, 2008.

American College of Radiology, Breast Imaging Reporting and Data System Atlas (BI-RADS Atlas), American College of Radiology, Reston, 2003.

10.

Giess

, Raza

, Birdwell

, Patterns of nonmasslike enhancement at screening breast MR imaging of highrisk premenopausal women, Radiographics, 33: 1343–1360, 2013.

11.

Health Quality Ontario, Cancer screening with digital mammography for women at average risk for breast cancer, magnetic resonance imaging (MRI) for women at high risk: an evidence-based analysis, Ontario Health Technol Assess Ser, 10; 1–55, 2010.

12.

Rosen

, Smith-foley

, DeMartini

, BI-RADS MRI enhancement characteristics of ductal carcinoma in situ, Breast, 13: 545–550, 2007.

13.

Liberman

, Morris

, Dershaw

, Ductal carcinoma on MR imaging of the breast, Am J Roentgenol, 181: 519–525, 2003.

14.

Morakkabati-Spitz

, Leutner

, Schild

, Diagnostic usefulness of segmental and linear enhancement in dynamic breast MRI, Eur Radiol, 15: 2010–2017, 2005.

15.

Pengel

, Loo

, Wesseling

, Avoiding preoperative breast MRI when conventional imaging is sufficient to stage patients eligible for breast conserving therapy, Eur J Radiol, 83: 273–278, 2014.

16.

Elston

, Ellis

, Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow up, Histopathology, 19: 403–410, 1991.

17.

American Joint Committee on Cancer, Manual for Staging of Cancer, Lippincott-Raven Publishers, Philadelphia, 1997.

18.

Wolff

, Hammond

, Schwartz

, American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor 2 testing in breast cancer, J Clin Oncol, 25: 118–145, 2007.

19.

Hurd

, Sneige

, Allen

, Impact of extensive intraductal component on recurrence and survival in patients with stage I or II breast cancer treated with breast conserving therapy, Ann Surg Oncol, 4: 119–124, 1997.

20.

Goldhirsch

, Winer

, Coates

, Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the primary therapy of early breast cancer, Ann Oncol, 24: 2206–2223, 2013.

21.

Esserman

, Hylton

, Yassa

, Utility of magnetic resonance imaging in the management of breast cancer: evidence for improved preoperative staging, J Clin Oncol, 17: 110–119, 1999.

22.

Liberman

, Morris

, Dershaw

, MR imaging of the ipsilateral breast in women with percutaneously proven breast cancer, Am J Roentgenol, 180: 901–910, 2003.

23.

Houssami

, Ciatto

, Macaskill

, Accuracy and surgical impact of magnetic resonance imaging in breast cancer staging: systemic review and meta-analysis in detection of multifocal and multicentric cancer, J Clin Oncol, 26: 3248–3258, 2008.

24.

Wapnir

, Anderson

, Mamounas

, Prognosis after ipsilateral breast tumor recurrence and locoregional recurrences in five National Surgical Adjuvant Breast and Bowel Project node-positive adjuvant breast cancer trials, J Clin Oncol, 24: 2028–2037, 2006.

25.

Clarker

, Collins

, Darby

, Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: and overview of the randomized trials, Lancet, 366: 2087–2106, 2005.

26.

Bedrosian

, Mick

, Orel

, Changes in the surgical management of patients with breast carcinoma based on preoperative magnetic resonance imaging, Cancer, 98: 468–473, 2003.

27.

Berg

, Gutierrez

, NessAiver

, Diagnostic accuracy of mammography, clinical examination, US, and MR imaging in preoperative assessment of breast cancer, Radiology, 233: 830–849, 2004.

28.

Bilimoria

, Cambic

, Hansen

, Bethke

, Evaluating the impact of preoperative breast magnetic resonance imaging on the surgical management of newly diagnosed breast cancers, Arch Surg, 142: 441–447, 2007.

29.

Deurloo

, Peterse

, Rutgers

, Additional breast lesions in patients eligible for breast-conserving therapy by MRI: impact on preoperative management and potential benefit of computerised analysis, Eur J Cancer, 41: 1393–1401, 2005.

30.

Bleicher

, Ciocca

, Egleston

, Association of routine preoperative magnetic resonance imaging with time to surgery, mastectomy rate, and margin status, J Am Coll Surg, 209: 180–187, 2009.

31.

Houssami

, Turner

, Morrow

, Preoperative magnetic resonance imaging in breast cancer: meta-analysis of surgical outcomes, Am Surg, 192(2013): 172–178.

32.

Fortune-Greeley

, Wheeler

, Meyer

, Preoperative breast MRI and surgical outcomes in elderly women with invasive ductal and lobular carcinoma: a population-based study, Breast Cancer Res Treat, 143: 203–212, 2014.

33.

Wang

, Kuntz

, Tuttle

, The association of preoperative breast magnetic imaging and multiple breast surgeries among older women with early stage breast cancer, Breast Cancer Res Treat, 138: 137–147, 2013.

34.

Vos

, Voogd

, Verhoef

, Benefits of preoperative MRI in breast cancer surgery studied in a large population-based cancer registry, Br J Surg, 2015, Oct 8; doi: 10 1002/bjs9947.

35.

Fancella

, Soro

, Castiglia

, Usefulness of magnetic resonance in patients with invasive cancer eligible for breast conservation: a comparative study, Clin Breast Cancer, 14: 114–121, 2014.

36.

Miller

, Abbott

, Tuttle

, The influence of preoperative MRI on breast cancer treatment,, Ann Surg Oncol, 19: 536–540, 2012.

37.

Davis

, Barth

Jr , Gui

, Use of MRI in preoperative planning for women with newly diagnosed DCIS: risk of benefit?, Am Surg Oncol, 19: 3270–3274, 2012.

38.

Allen

, Lago-Toro

, Hughes

, Is there a role for MRI in the preoperative assessment of patients with DCIS?, Am Surg Oncol, 17: 2395–2400, 2010.

39.

Peters

, van Esser

, van den Bosch

, Preoperative MRI and surgical management in patients with nonpalpable breast cancer: the MONET – randomized controlled trial, Eur J Cancer, 47: 879–886, 2011.

40.

Rauch

, Dogan

, Smith

, Outcome analysis of 9-gauge MRI-guided vacuum-assisted core needle breast biopsies, Am J Roentgenol, 198: 292–299, 2012.

41.

Jeh

, Kim

, Correlation of the apparent diffusion coefficient value and dynamic magnetic resonance imaging findings with prognostic factors in invasive ductal carcinoma, J Magn Reson Imaging, 33: 102–109, 2011.

42.

Lee

, Cho

, Kim

, Correlation between high resolution dynamic MR features and prognostic factors in breast cancer, Korean J Radiol, 9: 10–18, 2008.

43.

Chen

, Giger

, Bick

, Newstead

, Automatic identification and classification of characteristic kinetic curves of breast lesions on DCE-MRI, Med Phys, 33: 2878–2887, 2006.

44.

Sakamoto

, Tozaki

, Higa

, Categorization of non-mass-like breast lesions detected by MRI, Breast Cancer, 15: 241–246, 2008.

45.

Vag

, Baltzer

, Dietzel

, Kinetic characteristics of ductal carcinoma in situ (DCIS) in dynamic breast MRI using computer-assisted analysis, Acta Radiol, 51: 955–961, 2010.

46.

Camp

, McAuliffe

, Gilroy

, Minimizing local recurrence after breast conserving therapy using intraoperative shaved margins to determine pathologic tumor clearance, J Am Coll Surg, 201: 855–861, 2005.

47.

Orel

, Rosen

, Mies

, MR imaging-guided 9-gauge vacuum-assisted core-needle breast biopsy: initial experience, Radiology, 238: 54–61, 2006.

48.

Liberman

, Morris

, Dershaw

, MR imaging of the ipsilateral breast in women with percutaneously proven breast cancer, Am J Roentgenol, 180: 901–910, 2003.

49.

Schnall

, Blume

, Bluemke

, MRI detection of distinct incidental cancer in women with primary breast cancer studied in IBMC 6883, J Surg Oncol, 92: 32–38, 2005.