Annals of Surgical Oncology Cite Track
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10.1245/ASO.2004.12.008
Annals of Surgical Oncology 11:756-761 (2004)
© 2004 Society of Surgical Oncology
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ORIGINAL ARTICLES

Preoperative Magnetic Resonance Imaging Evaluation for Breast Cancers After Sonographically Guided Core-Needle Biopsy: A Comparison Study

Yun-Chung Cheung, MD, Yung-Liang Wan, MD, Yung-Feng Lo, MD, Wai-Man Leung, MD, Shin-Cheh Chen, MD and Swei Hsueh, MD

From the Department of Diagnostic Radiology (Y-CC, Y-LW), Chang Gung Memorial Hospital, College of Medicine, and School of Medical Technology; and Departments of Surgery (Y-FL, S-CC), Radiation Oncology (W-ML), and Pathology (SH), Chang Gung Memorial Hospital, Kwei Shan, Tao Yuan Hsien, Taiwan.

Correspondence: Address correspondence and reprint requests to: Shin-Cheh Chen, MD, Department of Surgery, Chang Gung Memorial Hospital, 5 Fu Hsing Road, Kwei Shan, Tao Yuan Hsien, Taiwan; Fax: 886-3-3330365; E-mail: alex2143{at}ms33.hinet.net


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The aim of the study was to evaluate the efficacy of contrast-enhanced magnetic resonance imaging (MRI) for preoperative assessment of palpable breast cancer after sonographically guided percutaneous core-needle biopsy.

Methods: Thirty-six breast cancers in 35 women that had been diagnosed by sonographically guided core-needle biopsy prior to subsequent MRI were evaluated in this retrospective study. Radiological and pathological reports, multiplicity, retroareolar involvement, and the size of the breast cancers were reviewed. The cancer sizes, as derived from sonography and enhanced MRI, were correlated with histological size in greatest diameter by means of Pearson’s correlation. The threshold value for significance was set at P < .05.

Results: Synchronous breast cancers were revealed in the index cases by means of enhanced MRI (10), sonography (8), and mammography (7). Two of the 36 index cancers (5.6%) benefited from MRI assessment. Retroareolar cancer extension was observed with enhanced MRI in five index cancers. Of these, one was also noted on both a sonogram and a mammogram. Four of the index cancers (11.1%) benefited from the enhanced MRI. Overall, five index cancers (13.9%) benefited from the enhanced MRI. With a gold standard of histology, the mean cancer sizes were underestimated by sonography and overestimated by enhanced MRI. In comparison with sonography, a stronger association was noted between MRI and histological measurements, with coefficients of 0.657 and 0.882, respectively (P < .001).

Conclusions: In a clinical setting, MRI for preoperative assessment of breast cancers is warranted. Minimally invasive, percutaneous core-needle biopsy did not alter the clinical efficacy of the MRI evaluation.

Key Words: Breast cancer • Conservative mastectomy • Magnetic resonance imaging • Needle biopsy • Preoperative planning • Sonography


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Sensitivities of 93% to 100% have been documented for contrast-enhanced magnetic resonance imaging (MRI) in the detection of breast cancer. Unfortunately, the specificity range varies widely (29–98%), depending on technique and patient selection.1,2 Morphological features and the intensity-time curve of the breast mass demonstrated by enhanced MRI can help to differentiate between the benign and malignant variants; however, accuracy is not guaranteed.3,4 Pathological diagnosis is impossible as well. This is one of the reasons why MRI is not utilized for every patient presenting with a palpable breast mass. The expense and time required for MRI examinations are other significant limitations, but the benefits of preoperative planning outweigh these to some extent. The cost-efficacy of MRI in clinical practice has thus been the subject of continuing discussion. In view of these efficiencies, enhanced MRI for preoperative cancer planning should ideally be performed after a definitive pathological diagnosis has been delivered.

Sonography is a valuable adjunctive modality, essential to fulfillment of the morphological criteria required for differential diagnosis of a palpable breast mass. Sonograms enable faithful distinction of the nature of a cyst or solid tumor.5,6 For certain solid tumors, however, histological differentiation of the benign and malignant variants is difficult. Sonographically guided core-needle biopsy is usually recommended for histological diagnosis before selection of management. For breast-cancer patients wishing to undergo conservative mastectomy, the multiplicity, extension, and size of breast cancers are important factors in preoperative planning. Over the past few years, sonography and enhanced MRI have proved to be important adjunctive modalities for achievement of this preliminary assessment. However, comparison of the effectiveness of sonography and enhanced MRI in postbiopsy evaluation of breast cancer has rarely been discussed. In this study, therefore, the efficacy of preoperative MRI assessment of palpable breast cancers, previously diagnosed by percutaneous sonographically guided core-needle biopsy, was assessed and analyzed.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Patients
Medical records for patients who underwent a total of 468 breast MRI examinations in our hospital from July 1998 to December 2002 were retrospectively reviewed. Forty of the patients with palpable breast masses had breast cancers diagnosed by sonographically guided core-needle biopsy prior to the breast MRI examination. Of these, 35 subjects subsequently underwent surgery at our hospital and 5 refused treatment at our hospital; mammographic examination was performed for all patients (26 at our institution and 9 at other hospitals). No fatty breasts were reported. Bilateral sonographic evaluations of whole breasts were performed to reveal features of the palpable masses and for preoperative assessment, including detection of synchronous masses and the extension and size of the index masses. After obtaining consent from the patients, we performed sonographically guided core-needle biopsy on the palpable index breast masses during the same examination session. In cases of breast cancer diagnosed by needle biopsy, MRI examination was subsequently arranged and performed within the following week, prior to the surgery.

Sonography and MRI Examination
A radiologist who specializes in breast imaging (CYC, who has greater than 5 years’ experience in sonography and sonographically guided core-needle biopsy and has done more than 300 breast MRI evaluations) performed the sonographic and MRI examinations in all cases. The multiplicity of the breast cancers, including multifocality (more than one focus in the same quadrant) and multicentricity (lesions involving more than one quadrant), was assessed. Regardless of whether the malignancies were multifocal or multicentric, all were defined as synchronous cancer on the basis of the criterion of being isolated cancer independent of the index breast cancer (i.e., the target of the sonographically guided core-needle biopsy), separated by at least 1 cm. Additionally, the extension of the breast cancer was evaluated, and the size of the breast cancer was measured in greatest diameter.

Sonography with a broadband linear-array transducer (5~9 MHz; Elegra; Siemens, Issaquah, WA) was used for bilateral whole-breast examination, with axial and sagittal arrays used in all cases. The index cancers were carefully evaluated from radial and antiradial orientations. After recording the sonographic features and sizes of the index breast cancers, as well as determining the presence of synchronous tumors, we performed sonographically guided core-needle biopsy, using a powerful automatic spring-loaded biopsy gun (Magnum; C. R. Bard, Covington, GA) and an 18-gauge cutting biopsy needle (C. R. Bard) with a 22-mm throw. The specimens were then stored in formalin solution and sent for histopathological examination.

After the histological diagnoses of breast cancer, all patients underwent dynamic enhanced MRI examination with a 1.5-T MR scanner with dedicated bilateral breast coils (MagnetomVision; Siemens, Erlangen, Germany) while in the prone position to ensure good imaging intensity. The image-acquisition protocol, including the pulse sequence and the number, thickness, and location of slices, was kept the same. Cancer detection was based on dynamic enhanced MRI, with use of the three-dimensional turbo fast low-angle shot (FLASH) pulse sequence in an axial plane. Both breasts were examined simultaneously. Dynamic imaging was performed with 14 continuously repeated sequences, including four precontrast and 10 postcontrast dynamic acquisitions. The dose of contrast agent (Magnevist; Berlex, Montville, NJ) was based on body weight (0.1 mmol/kg). The injection was commenced after completion of the four precontrast acquisitions at a constant rate, finishing at precisely 15 seconds for all patients.

Demonstration of index and synchronous breast cancers was based on the raw image data, as well as subtraction of the images at 2 and 4 minutes after gadolinium injection. Discrete enhanced masses, with patch or linear enhancement extending to 1 cm beneath the nipple-areolar region, were classified as retroareolar involvement. The cancer size was measured from the greatest diameter on the axial plane of the enhanced images at approximately 2 minutes. The multiplicity and retroareolar extension of the breast cancers were assessed.

Histological Correlation
Cancer size, presence of synchronous cancers, and cancer involvement were based on official reports from the pathology department. The histological cancer size was measured in the long axis of the mass. Regardless of whether the location was multifocal or multicentric, a synchronous breast cancer was defined as any other malignancy completely separate from the index growth.

Statistical Analysis
Our data were retrospectively analyzed on the basis of official reports from the radiology and pathology departments. The presence of synchronous cancers and the extent of retroareolar involvement were recorded from the mammograms, sonograms, and MRI. The mean cancer sizes, as measured with sonography, enhanced MRI, and histology, were calculated and analyzed with paired t-tests. Additionally, the sizes of the malignancies, as measured with sonography and MRI, were individually correlated with the measurements from pathology by means of Pearson’s correlation, with statistical significance set at P < .05.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In this clinical setting, 35 women (age range, 28–67 years; average, 43.8 years) with 36 palpable breast cancers were enrolled. One patient had bilateral breast carcinoma. Final histological diagnoses were invasive ductal carcinoma (n = 24), ductal carcinoma in situ (n = 5), medullary carcinoma (n = 2), tubular carcinoma (n = 2), mucinous carcinoma (n = 1), invasive lobular carcinoma (n = 1), and mixed ductal and lobular carcinoma in situ (n = 1). Sixteen cancers were detected in the right breast and 20 in the left. Modified radical mastectomy was used to excise 21 of the cancers, and conservative mastectomy was performed for 15. Axilla lymph node sampling or dissection was undertaken in all cases, with metastasis revealed in 13.

Multifocal/multicentric and Retroareolar Extension of Breast Cancer
Of these 36 index cancers, synchronous breast cancers were detected by mammography for 7 (19.4%), sonography for 8 (22.2%), and contrast-enhanced MRI for 10 (27.8%). The histological subtypes of the index breast cancers with synchronous malignancies, as observed on sonogram, were invasive ductal carcinoma (n = 4), ductal carcinoma in situ (n = 3), and mixed invasive ductal and lobular carcinoma in situ (n = 1). Two of the 10 index breast cancers with synchronous cancer (20%) were additionally detected on enhanced MRI. The histological subtypes of these two cancers were invasive ductal carcinoma and tubular carcinoma. However, the overall percentage of synchronous breast cancers detected only by enhanced MRI was just 5.6% of all the index cancers.

Retroareolar extension was noted in five index breast cancers by means of enhanced MRI. Of these, one was also demonstrated on both a sonogram and a mammogram. On the enhanced MRI, the cancer extended to the retroareolar region, revealing linear enhancement (n = 2; Fig. 1), patchy enhancement (n = 2; Fig. 2), and discrete masses (n = 1; Fig. 3). Of the 36 index cancers, the MRI examination was of significant benefit for four (11.1%). The histological subtypes of these four cancers were ductal carcinoma in situ (n = 2), invasive ductal carcinoma (n = 1), and invasive lobular carcinoma (n = 1). Of these, nipple involvement was proven histologically for two.



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FIG. 1. Subtracted enhanced MRI shows an enhanced cancer in right breast, with linear enhancement of the retroareolar region and nipple. Finally, the nipple was proved to be involved.

 


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FIG. 2. Subtracted enhanced MRI shows a large patch of enhancement converging to the retroareolar region of the right breast. The final diagnosis of the index mass was invasive ductal carcinoma that was infiltrating with atypical ductal hyperplasia and lobular carcinoma in situ. The skin and nipple were invaded.

 


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FIG. 3. Subtracted MRI shows multiple enhanced cancers in the outer region and the retroareolar region of the right breast.

 
Tumor-Size Correlation with Sonogram, MRI, and Histology
The breast cancers ranged in size from 1 to 4 cm and 1 to 7 cm, on the basis of sonography and enhanced MRI, respectively. By contrast, the documented sizes of the pathology specimens ranged from 1 to 8 cm. The means of cancer sizes, as measured by sonography and MRI, were 2.067 cm (standard error, 0.12; P = .673) and 2.32 cm (standard error, 0.194; P = .069), respectively. The mean size of the pathology specimens was 2.133 cm (standard error, 0.21). The sonography measurement was closer to the pathology analog than to the enhanced MRI measurement; the average underestimation was 0.066 cm with the former and the average overestimation was 0.187 cm with the latter. As determined by Pearson’s correlation, both imaging modalities yielded statistically significant measurements in terms of correlation with actual pathological size, with coefficients of 0.657 for sonography and 0.882 for enhanced MRI (P < .001 for both; Figs. 4 and 5Go).



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FIG. 4. Linear regression line of cancer size as determined by sonography and pathology.

 


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FIG. 5. Linear regression line of cancer size as determined by enhanced MRI and pathology.

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Conservative mastectomy is satisfactory for most breast cancers. However, complete resection is mandatory to prevent recurrence. Previous studies have shown that 30% to 63% of mastectomy specimens are multifocal or multicentric7,8; therefore, an evaluation for synchronous cancer after diagnosis is important before conservative mastectomy is performed. Precise preoperative information about the multiplicity, extension, and size of the tumors should be obtained before the selection of a surgical alternative.

Palpation is not sufficiently reliable in detecting small breast cancers, and imaging underpins the evidence-based, decision-making process. Although mammography is the fundamental breast-imaging modality, its sensitivity for cancer deteriorates in dense breasts. Furthermore, approximately 10% to 15% of palpable breast cancers are not visible on mammograms.9 For patients with a palpable mass, sonography remains the best and most convenient imaging modality for distinguishing cysts from solid tumors and for differentiating benign and malignant variants.10 With the advantage of real-time, high-resolution imaging, sonographically guided core-needle biopsy is relatively straightforward and highly accurate.11 Invasive procedures should be avoided before imaging evaluation is complete, and histological diagnosis is always the final step prior to mastectomy. Pathological proof of breast cancer eliminates the expense of unnecessary MRI in cases in which the tumor or process is benign. Enhanced MRI examination, before or after needle biopsy, remains controversial. Given our results, we suggest that enhanced MRI still merits consideration.

In our hospital, breast sonography is an initial tool to identify or differentiate breast tumors. Adjunctive sonographic screening is clinically valuable because it increases the overall detection of cancers in dense breasts by 17% and improves the detection of asymptomatic malignant tumors with imaging alone by 37%.12 In detecting multifocal breast cancers, sonography has a reported accuracy rate of 83%13; however, this result is operator-dependent. Some have proposed that enhanced MRI is the best modality for detecting multifocal or multicentric breast cancers because of its high sensitivity.14 In one study, MRI depicted additional unsuspected tumors in approximately 33% of patients with breast cancer,15 and therapeutic changes based on MRI findings have occurred in 11% to 20% of patients examined.14–16 Another investigation demonstrated that 93% of patients gained no advantage from enhanced MRI after mammography and sonography.17 In a series of percutaneously proved cancers, additional ipsilateral, mammographically occult cancers were identified in 27%.18 In our sample, enhanced MRI was useful in 13.9% of all index breast cancers, with benefits including the detection of synchronous cancer (5.6%) and the demonstration of retroareolar cancer extension (11.1%).

Although there is no definitive size criterion for conservative mastectomy, this procedure may be less suitable for tumors larger than 3 cm.19 The accuracy of preoperative mammography, sonography, and enhanced MRI in measuring tumors has been compared. Enhanced MRI is reportedly superior to sonography and mammography, with correlation coefficients of 0.93, 0.92, and 0.84, respectively,20 and with correlation coefficients of 0.98, 0.46, and 0.45, respectively.21 The correlation between size on pathological analysis and size on enhanced MRI is statistically significant, particularly for large breast cancers or postchemotherapeutic analogs.21,22 In our series, the relationship between imaging size and pathological size of the index cancers was statistically significant for both sonography and enhanced MRI. Measurement accuracy with enhanced MRI seems to be preserved despite the use of core-needle biopsy.

In comparisons of the mean sizes of the cancers, sonographic measurements were more accurate than enhanced MRI measurements with respect to the histological standard. Size was underestimated with sonography and overestimated with enhanced MRI, a finding seemingly incompatible with the derived correlation coefficients. With sonography, measurement is based on lesion morphology, whereas with enhanced MRI, it is based on the area of contrast enhancement.23 The enhancement of a cancer depends on angiogenesis, which cannot be observed with sonography.24 On the other hand, the enhancement technique improved the accuracy of MRI (relative to mammography and sonography) in assessing cancer extension,25 particularly in larger malignancies or index cancers surrounded by an area of infiltration. The poorer sonographic discrimination in many of our larger cancers resulted in a correlation coefficient lower than that of enhanced MRI in our case-by-case analysis.

Routine MRI evaluation is not necessary for all cases of breast cancer. In our study, 13.9% of all index cancers benefited from MRI in comparison with sonography. Although sonography is highly sensitive in evaluating palpable masses, some multifocal cancers can be missed because of their small size or because of differences in subjective observation. Underestimation of the extent of disease with sonography is also common because of intraductal spread and poor resolution in the retroareolar region. In detecting synchronous breast cancer, assessing retroareolar cancer extension, or measuring the size of the lesions, MRI was superior to both sonography and mammography in our sample. However, more-precise criteria should be established to identify individuals for whom enhanced MRI is essential. Multicenter investigations in larger populations are needed. From a cost-effectiveness perspective, enhanced MRI should be encouraged for the preoperative assessment of breast cancer after minimally invasive core-needle biopsy is performed.


    FOOTNOTES
 
Minimally invasive percutaneous needle biopsy did not alter the clinical efficacy of preoperative MRI evaluation of breast cancers in providing additional information for the detection of synchronous cancer and the retroareolar extent of cancer, and a good correlation between MRI and histological size was noted.

Received for publication December 3, 2003. Accepted for publication April 21, 2004.


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 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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