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1 Department of Radiology, Johannes Gutenberg University Hospital,
Langenbeckstr. 1, 55131 Mainz, Germany.
2 Department of Gynecology, Johannes Gutenberg University Hospital, 55131 Mainz,
Germany.
Received August 29, 2001;
accepted after revision May 30, 2002.
Preliminary results presented at the annual meeting of the American
Roentgen Ray Society, New Orleans, May 1999.
Abstract
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SUBJECTS AND METHODS. One hundred four women (age range, 34-84 years; mean age, 60 years) with findings highly suggestive of malignancy in the breast were examined with mammography, sonography, and dynamic MR imaging before undergoing surgery. All visualized suspicious lesions were correlated histologically. The diagnostic relevance of sonographic and MR imaging findings was compared with the diagnostic value of the findings of clinical examination and mammography alone.
RESULTS. Twenty-seven tumors showed multifocal or multicentric invasive growth at pathology. Of these 27, 48% were correctly diagnosed via mammography alone; 63%, via the combination of mammography and sonography; and 81%, via MR imaging. Nine of the index tumors were invisible on mammography but were detected on sonography. Use of sonography benefited 13 patients and produced two studies with false-positive findings. Use of MR imaging benefited seven patients and produced eight studies with false-positive findings. In summary, 93% of all patients gained no advantage from MR imaging. Relevant additional findings were significantly more frequent in patients with dense breasts.
CONCLUSION. Although MR imaging is most sensitive for the detection of small tumors, routine preoperative MR imaging appears to be unnecessary for most patients if a combination of mammography and whole-breast sonography is used. Additional MR imaging can be restricted to problematic cases in women with dense breast parenchyma.
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Despite its high sensitivity for the detection of malignant breast lesions, MR imaging does not qualify as a screening method because it is time-consuming and expensive. The type of patients in whom MR imaging would be most helpful in selecting an appropriate treatment or in improving outcomes has not yet been determined. Currently, MR imaging is chiefly used for the detection of malignancy or to rule out the presence of malignancy in patients with postoperative formation of scar tissue or with breast implants when findings from mammography are indeterminate. MR imaging has been recommended for preoperative staging of breast cancer, especially for determining multifocality (lesions with more than one intraductal or invasive focus) and multicentricity (lesions involving more than one quadrant of the breast) [1, 2]. Several studies have shown that MR imaging has a higher sensitivity than mammography in the detection of multifocal or multicentric tumor lesions [3,4,5,6,7,8]. The question is whether MR imaging should be included in the routine workup of patients with suspected breast cancer. Breast sonography is another valuable adjunctive modality to mammography [9], but as yet little data comparing breast sonography with MR imaging are available.
In our study, we compared mammography and bilateral whole-breast sonography with MR imaging in the preoperative evaluation of suspected mammary carcinomas, with special attention to the influence on treatment.
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Clinical Examination, Mammography, and Sonography
In all patients, existing mammograms (obtained at outside institutions)
were reviewed by a radiologist experienced in breast imaging. New mammograms
(Senographe DMR; General Electric Medical Systems, Milwaukee, WI) in two
projections were obtained for patients whose available mammograms had been
obtained more than 1 month earlier or were not of sufficiently high quality.
Mammographic findings were evaluated according to the Breast Imaging Reporting
and Data System (BI-RADS) of the American College of Radiology
[10]. Parenchymal density on
mammograms was assessed using a modification of the method described by
Stomper et al. [11]. A score
of 1 was used for breasts composed of less than 10% dense tissue; 2, for those
containing 10-24%; 3, for those containing 25-49%; 4, for those containing
50-80%; and 5, for those containing more than 80% dense tissue.
The same radiologist subsequently performed clinical and sonographic examinations. Sonography (Toshiba SSA 250 with an 7.5-MHz annular array transducer; Toshiba, Tokyo, Japan) was performed with axial and sagittal scanning of both breasts. Suspicious areas, such as palpable, mammographic, or sonographic abnormalities, were also scanned in a radial and antiradial orientation with and without compression. Criteria for malignancy were solid lesions with ill-defined or irregular borders, noncalcified lesions with posterior acoustic shadowing, architectural distortions, and solid intracystic or intraductal lesions. In accordance with the routine workup of suspicious breast findings at our institution, we based a patient's final imaging diagnosis on the combination of the clinical, mammographic, and sonographic findings. In patients with multifocal or multicentric tumors, the distances between the main tumor and any additional lesions were measured.
MR Imaging
Informed consent was obtained from all patients (those with
contraindications had been excluded). The study protocol had been approved by
the institutional review board. MR imaging was performed on a 1.0-T scanner
(Magnetom Impact Expert; Siemens, Erlangen, Germany) using the manufacturer's
double breast coil with the patient in the prone position. T2-weighted MR
images were acquired first— either a half-Fourier single-shot turbo
spin-echo (HASTE) sequence (axial orientation; TR/TE, 5432/90; field of view,
350 x 350 x 100 mm; and matrix, 256 x 252 x 29) or a
three-dimensional double-echo steady-state sequence (coronal orientation;
15/7; flip angle, 30°; field of view, 350 x 175 x 119 mm; and
matrix, 256 x 96 x 64).
The main part of the examination was a dynamic three-dimensional contrast-enhanced T1-weighted fast low-angle shot sequence (coronal orientation; 15/7; flip angle, 30°; field of view, 350 x 175 x 119 mm; and matrix, 256 x 96 x 64) with an acquisition time of 93 sec and a spatial resolution of 1.37 x 1.82 x 1.86 mm. One set of T1-weighted MR images was acquired before and five sets were acquired after manual administration of a bolus of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) at a dose of 0.1 mmol/kg of body weight into a cubital vein followed by a 20-mL saline flush. The injection was administered during a 5-sec break between the measurements.
We used the manufacturer's software to subtract the unenhanced images from the first and third contrast-enhanced studies in order to visualize both early- and late-enhancing lesions. Using an image analysis software package (MRVision; MRVision, Menlo Park, CA), we calculated the intensity—timecurves for the enhancing lesions in regions of interest placed in areas of maximum enhancement. We also used software (VRS-800XS and VRS-APP; ISG Technologies, Mississauga, Ontario, Canada) to generate axial and sagittal reconstructions of both breasts of the patients to improve lesion visualization and localization.
MR imaging findings were interpreted through consensus by two radiologists who were experienced in breast imaging and who were aware of all clinical, mammographic, and sonographic findings. A lesion was suspected to be a malignancy if it showed a focal signal that enhanced 100% or more in the first or second contrast-enhanced T2-weighted MR study or had washout (decrease in signal intensity of at least 10% during the last three contrast-enhanced T2-weighted studies). Enhancing lesions that had spiculated or irregular borders or that had unilateral enhancement that lacked clear borders were also considered suspicious. Lesion size was measured as the largest diameter of the enhancing region.
Histology
Regardless of the modality by which the suspicious lesions were detected,
all were surgically removed. Nonpalpable lesions were localized using
mammographic or sonographic guidance to place a guidewire. For lesions that
were visible only on MR imaging with no correlation on sonography (even on a
repeated examination with the examiner being aware of the MR imaging
findings), we used CT guidance to place a guidewire with the patient in the
supine position after reproducing lesion enhancement with an IV contrast agent
(Ultravist 300; Schering)
[12]. If tumor-free margins of
at least 1 cm could not be achieved, a secondary surgical resection was
performed. Specimens were marked with ink to identify anterior, posterior,
cranial, and caudal margins in relation to the patient. Specimen processing
and interpretation were performed by pathologists with experience in breast
disease. All macroscopically suspicious areas as well as all
guidewire-localized specimens were serially sectioned and stained in slices as
large as 5 x 5 cm. In patients in whom mastectomy specimens were
obtained, additional samples were taken from all breast quadrants and from the
retroareolar region. Histologic findings and imaging results were correlated
by pathologists and radiologists in conference.
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The mean histologic size of the index lesion was 21 mm (SD, ± 15 mm); the size range was from 6 to 100 mm. Of the malignant tumors, the histologic staging was T1 in 60 patients (59%), T2 in 36 patients (36%), and T3 or T4 in five patients (5%). Thirty-four patients underwent mastectomy, whereas the others underwent a quadrantectomy or wide local excision. Histologic measurements of tumor size agreed with 62% of the mammographically derived measurements of tumor size, 77% of the sonographically derived measurements, and 71% of the MR imaging—derived measurements (size tolerance, ±5 mm, because the lesion size was recorded in steps of 5 mm).
Eight patients had mammographically invisible index lesions that were detected on sonography (mean lesion size, 12.8 mm; size range, 9-21 mm). In these patients, mammography showed no abnormality in dense breasts or showed an asymmetric parenchymal density with no detectable mass. MR imaging did not add any relevant information regarding the index lesions to the information gained through sonography in these patients. One of the lesions was a 10-mm papilloma that gave false-positive results on both sonography and MR imaging.
Contralateral Breast
In 13 patients (13%), a biopsy was performed on the contralateral breast
because of a suspicious finding. Histology revealed three invasive
malignancies, one DCIS, and nine cases of benign breast changes. A 15-mm
tubular carcinoma and a 12-mm invasive ductal carcinoma were detected on
mammography and confirmed on sonography and MR imaging. A 6-mm invasive
ductal—lobular carcinoma was suggested in one mammographic projection
but could not be identified in the second projection. MR imaging clearly
showed the lesion as being located close to the thoracic wall. Sonographic
findings were negative on the first examination; however, because we were
aware of the MR findings, we identified the lesion and used a guidewire to
localize it. A 10-mm DCIS was visualized on MR imaging only. Retrospective
sonography showed a corresponding hyperechogenic lesion with smooth borders
that appeared to be benign. Of the nine biopsies that revealed benign results
(two papillomas, three cases of fibrocystic changes, two cases of intraductal
hyperplasia, and two cases of atypical intraductal hyperplasia), four were
performed because of suspicious findings on mammography or sonography (two
cases of microcalcifications, one mammographic mass with no correlation on
sonography, and one case of solid intracystic structures seen on sonography),
and five were performed because of suspicious enhancement on MR imaging (Fig.
1A,1B,1C,1D,1E,1F,1G,1H).
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Multifocal and Multicentric Tumors
Of 101 patients with malignant tumors, histology showed multiple invasive
lesions in 27 (27%). Furthermore, histology showed five separate foci of DCIS
(size range, 1-7 mm) in one patient with and in four patients without
multifocal invasive disease. Thus, a total of 31 patients (31%) were found to
have an additional invasive or noninvasive tumor at histology. The five DCIS
tumors were found at histology alone; none of them had been visible on any
imaging modality.
Cases of multifocal invasive tumors were divided into two groups: group 1 was composed of the 17 patients who had one to three distinct additional foci, and group 2 was composed of the 10 patients with multiple (more than three) additional foci. In group 1, a total of 25 lesions were identified at histology in addition to the index lesions. Mammography alone revealed 11 lesions (sensitivity, 44%), mammography with sonography revealed 15 lesions (sensitivity, 60%), and MR imaging revealed 21 lesions (sensitivity, 84%). In group 2, the index tumors were four invasive ductal carcinomas, three lobular carcinomas, two ductal—lobular carcinomas, and one tubular—lobular carcinoma. The size of the individual additional lesions was equal to or less than 10 mm in all patients, and the radius in which the additional lesions were found from the main tumor was at least 3 cm. The patients in this group were regarded as unsuitable candidates for breast-conserving treatment (Fig. 2A,2B,2C,2D,2E,2F,2G,2H,2I,2J,2K). Underestimated on all modalities was one disseminated lobular carcinoma in situ with early multifocal invasion as well as one lobular invasive carcinoma with multiple invasive foci that were only a few millimeters from the main tumor.
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In summary, of the 27 patients with multifocal or multicentric tumors, 13 had conditions correctly diagnosed from mammographic findings alone; 17, from mammographic and sonographic findings combined; and 22, from MR imaging findings (Table 1). Twenty-three of these 27 patients had already been examined at other institutions with mammography or combined mammography and sonography before being referred to our institution. We suspected multifocality or multicentricity in seven (30%) of the 23 patients on the basis of the written imaging reports; however, after reviewing the patients' mammograms and repeated sonograms, we suspected multifocality or multicentricity in 16 (70%) of the 23 patients.
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False-Negative Findings on MR Imaging
Ten histologically proven malignant lesions were not revealed on MR
imaging. One index tumor (18-mm invasive ductal carcinoma) was not
distinguishable from the surrounding parenchyma because of massive diffuse
enhancement in a premenopausal patient. This tumor was well visualized on
mammography and sonography. Four small, distinct invasive carcinomas
(presenting as foci distant from the main tumor) were not revealed on any
method. These were two invasive lobular carcinomas with diameters of 1 and 7
mm, and two invasive ductal carcinomas with diameters of 1 and 2 mm. As was
mentioned earlier, five DCIS tumors (size range, 1-7 mm) were also not
detected on any modality.
Influence on Treatment Decisions
In a retrospective analysis, we identified 15 patients with
treatment-relevant findings visualized on sonography that were not detected on
mammography. In two patients, additional biopsies were performed for lesions
that appeared suspicious on sonography but were benign at histology. The other
cases included the nine patients with mammographically invisible index tumors.
In another four patients with multifocal or multicentric tumor foci,
sonographic findings led to an increased resection volume or an additional
biopsy. Of these 13 patients who benefited from sonography, only two had a
change in diagnosis attributable to MR imaging. In one patient, a
treatment-relevant additional tumor focus was found (2 cm from the index
tumor). In another, MR imaging showed additional foci close to the index
tumor, but these findings had no impact on treatment decisions.
MR imaging, on the other hand, showed 19 suspicious lesions in 18 patients that either had not been visualized or had been considered probably benign on mammography and sonography. At histology, nine corresponding malignant lesions were found (one contralateral invasive carcinoma, one contralateral in situ carcinoma, and seven ipsilateral additional invasive foci in six patients). The diameters of these tumors were between 5 and 10 mm, with a mean diameter of 7 mm. The remaining 10 lesions were benign.
To determine the clinical value of MR imaging compared with mammography and sonography, we performed a case-oriented analysis. MR imaging was judged to give the best impression of tumor location and extent in 13 patients, but the findings caused no change in treatment. In seven patients, MR imaging did lead to a change in treatment (larger resections or mastectomies in five patients and contralateral resections in two patients) because additional tumors were identified. On the other hand, MR imaging gave less information than mammography and sonography in eight patients. The reasons for the decreased information were nonspecific diffuse parenchymal enhancement or artifacts that masked tumors (five patients) and the inability of MR imaging to reveal a tumor that presented only with microcalcifications (three patients). In another eight patients, unnecessary contralateral biopsies or larger ipsilateral resections were prompted by false-positive findings on MR imaging (Table 2).
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Breast Density
The distribution of mammographic density scores was as follows: 1 in eight
patients (8%), 2 in 21 patients (20%), 3 in 34 patients (33%), 4 in 27
patients (26%), and 5 in 14 patients (13%). The mean breast density score was
3.17. Forty-one patients (39%) had scores of 4 or 5, indicating that at least
50% of the breast tissue was dense. The 13 patients who had mammographically
invisible tumors visualized on sonography had a mean breast density score of
3.92. The difference between this group and all patients was statistically
significant (p < 0.01, Wilcoxon's rank sum test). The seven
patients with treatment-relevant additional tumors found on MR imaging had a
mean density score of 4.00. Combining the scores of these patients together
with those of the 13 patients in whom MR imaging did not change treatment
decisions but did give the best image of the tumor, the mean density score was
3.60 (as compared with all patients; p = 0.05, Wilcoxon's rank sum
test).
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We compared sonography and MR imaging as adjunctive imaging techniques to mammography. Our study population consisted of consecutive patients, 95% of whom had T1 or T2 tumors and were suitable candidates for breast conservation. This arrangement represented a realistic clinical situation, in contrast to prior studies that focused on patients with large tumors who usually underwent mastectomies [4, 7].
The exact measurement of the size of the index tumor has only limited clinical relevance because no precise size limit for breast-conserving surgery has been established. Even tumors larger than 2 cm can be treated successfully using breast conservation if sufficient surrounding tissue is available to obtain free margins. Although the treatment decision depends on the size of the breast and the location of the lesion, many tumors with a diameter of more than 3 cm are less suitable for breast-conserving surgery [13]. Mammography has a small geometric magnification factor, and the largest cancer axis may be oblique to the projection plane. In addition, tumor borders may be poorly demarcated, especially in dense breasts [15, 16]. Sonography and MR imaging are multiplanar techniques that allow an accurate determination of the maximal diameter of a lesion. Measurement of the diameter on sonography is based on lesion morphology, whereas the size of a lesion on MR imaging is usually measured as the diameter of the contrast enhancement, which reflects the hypervascularized tissue [15]. Histology is the gold standard, but measurements can also be inaccurate if the cut plane is not parallel to the maximal diameter of the tumor. In our study, measurements derived from MR imaging and sonography correlated better with histology than those derived from mammography, but MR imaging was not superior to sonography. These findings are consistent with those of Yang et al. [16].
In our experience, however, large tumors or tumors in very dense breasts are often best visualized on MR imaging. Sonography has a limited field of view and can only show certain details of a tumor in every image, but MR imaging data can be reformatted with multiplanar reconstruction or maximum intensity projection to display the whole tumor in its relation to the remaining breast, chest wall, and axilla. The overview given by these images was found to be helpful by our surgeons in several patients.
In our study, we observed four of 101 synchronous contralateral carcinomas. MR imaging confirmed one suspected 6-mm invasive carcinoma and found one in situ carcinoma not detected on the other modalities and, thus, gave valuable additional information for 2% of the women. Because of the low prevalence of contralateral disease, these data are of limited statistical relevance. Contralateral tumors are usually detected on regular contralateral mammography, which is mandatory for the follow-up of patients with breast cancer [17]. If some of these mammographically occult tumors could be detected on sonography or MR imaging at the same time as the primary tumor is found, patients could be spared a second operation, and perhaps a smaller contralateral resection would be possible. However, the overall prognosis of patients is not impaired as long as the secondary tumor is at the same stage or a lower stage than the primary carcinoma [18].
In their study of 336 patients, Fischer et al. [8] reported 15 patients (4%) with synchronous contralateral tumors found on MR imaging alone. Seven of these tumors ranged from 10 to 16 mm. Some of these types of tumors might theoretically be visible on sonography. In our study, all tumors larger than 1 cm were detected using the combination of mammography and sonography, but it is probably faster and easier to detect a focal enhancement on MR imaging than a small tumor on sonography, especially in inhomogeneous tissue. Identifying small tumors on sonography depends on the skill of the operator and the availability of high-quality equipment.
Many mammary carcinomas present as multifocal (defined as more than one focus in the same quadrant of the breast) or multicentric disease (involving more than one quadrant) [19]. The concept of quadrants has limitations in clinical use because the borders of the quadrants are not anatomically defined and no precise information about the intertumor distance is conveyed. In our study, we recorded the number and the size of the additional lesions and the distance between the satellite lesions and the index tumor. In histopathologic studies of mastectomy specimens, investigators found residual malignancy beyond a 5-cm zone around the index tumor in 30-40% of patients [19]. Holland et al. [20] concentrated on stage T1 and T2 carcinomas that would have been suitable for breast-conserving surgery. In 63% of their patients, they found additional foci. In 43% of these patients, the additional foci were outside a radius of 2 cm relative to the index lesion, and in 10%, the foci were outside a radius of 4 cm.
The sensitivity of mammography for the detection of multifocal and multicentric tumors ranges between 15% and 45% [3, 5, 6, 21]. Sonography has been shown to be useful as a complement to mammography and as a method of detecting additional, occult tumors [9, 22]. In our study, the addition of sonography to mammography increased the sensitivity for multifocality from 48% to 63%. No tumor foci larger than 1 cm were overlooked on sonography.
In correlation with the literature, MR imaging was the most sensitive modality, with a sensitivity of 81%. Our results do not corroborate the findings of a 100% sensitivity for MR imaging reported by researchers in small [2] and large [8] series. Failure of MR imaging to reveal certain tumors in our study was caused by artifacts, background enhancement, and the extremely small size of the tumors (four invasive tumors with a mean size of 3 mm). These small tumors came close to the limits of spatial resolution of MR imaging. In addition, tumors with a volume of a few cubic millimeters can receive their vascular supplies by means of diffusion and may not yet have induced the substantial neoangiogenesis necessary to detect lesion enhancement on MR imaging [23]. Similarly, small in situ carcinomas cannot be excluded by MR imaging; this finding agrees with those reported by several other authors [24, 25]. Because such lesions may be detected only at histology, more small occult tumors probably remain in the surgically treated breast.
We do not know whether small foci of a residual tumor remaining in the breast after breast-conserving surgery influence the recurrence rate or a patient's prognosis. Despite the existence of subclinical multifocality in patients with breast cancer, several trials have found no significant difference in overall survival rate between patients treated with mastectomy and those treated with breast-conserving surgery [26, 27]. Significant differences were seen in the rate of local recurrences after breast-conserving surgery, depending on the use of radiation therapy. Although patients who received radiation therapy to the breast after conservative surgery had no higher risk of recurrence than patients who underwent mastectomy (5-10% in 10 years), the risk of recurrent disease was fourfold higher in patients who had conservative surgery but received no radiation [28, 29].
The observed rate of recurrence in patients who had no radiotherapy correlates well with the expected histologic incidence of multifocality (30-40%), a finding that implies that a residual tumor may become a starting point for a recurrence of breast cancer and that radiotherapy is capable of destroying the residual foci. Confirmation of this point is provided by the observation that patients undergoing gross tumorectomy in which the need for clear margins is not emphasized who subsequently receive a local radiation boost do not have an increased rate of recurrence [30, 31]. However, the incidence of recurrent tumors may depend on the ratio of the amount of residual tumor cells and the dose of radiation. In our study, only tumors measuring less than 1 cm were missed with the combination of mammography and sonography. It is possible that all these tumors could be destroyed by radiation therapy, in which case the prognosis would not change regardless of whether additional studies with MR imaging are obtained. However, further studies and long-term observation periods are needed to address this issue.
The incidence of patients who had additional tumor revealed only on MR imaging and whose treatment was changed because of findings on MR imaging is relatively low. In our study, 93% of all patients had no treatment-relevant additional information revealed on MR imaging. Even in the 13% of patients in whom a more comprehensive display of the tumor was useful to the surgeons, the basic operative approach was not changed. In principle, this finding means that routine mammography and sonography are sufficient for most patients, and the additional cost of MR imaging can be saved. However, the 7% of patients who have additional tumors revealed only on MR imaging need to be identified. We found a correlation between increased mammographic breast density and treatment-relevant additional findings on sonography and on MR imaging. However, relevant findings on sonography were not a predictor for additional relevant findings on MR imaging. Mammograms of patients with dense breasts are generally more difficult to interpret, and tumors can be masked by dense tissue [32]. In our experience, sonography can also be impaired by inhomogeneous tissue, as is seen in breasts with extensive fibrocystic changes. The results suggest that MR imaging may be most effective when used as a tertiary imaging method in patients with dense breast parenchyma on mammography, inhomogeneous tissue on sonography, or both.
The main disadvantage of MR imaging is false-positive findings (8% of our patients) that lead to unnecessary additional biopsies. Other authors have reported rates of false-positive findings from MR imaging as high as 57% [3]. An unnecessary biopsy with an additional tissue defect may produce a negative cosmetic result, and the scar tissue from the procedure can lead to future diagnostic problems. Furthermore, localizing and obtaining biopsy specimens from lesions only visible on MR imaging are costly and time-consuming, although several improved techniques have been recently proposed [33,34,35,36]. No simple method of confirming successful lesion removal exists, because enhancement depends on vascular perfusion. These circumstances limit the routine use of MR imaging. Improving the specificity of MR imaging should be the focus of further studies. In our experience, additional criteria, such as lesion morphology, are of only limited significance in small lesions.
We detected substantially more multifocal or multicentric tumors in the patients in our study than did the examiners in medical offices; we base this assessment on the written notes accompanying some patients. Of course, the aim of office-based mammographic screening is to identify patients who need a surgical referral rather than to find all multicentric lesions. Therefore, if improvements in patient positioning or operator technique could result in better image quality, repeated mammograms should be obtained. On the basis of our results, we suggest that bilateral whole-breast sonography be performed for preoperative planning, with special attention given to the possible presence of extremely small lesions.
In summary, we propose whole-breast sonography as the first-line complementary imaging modality to mammography in the preoperative examination of women with breast cancer who are considered candidates for breast conservation. The routine use of MR imaging appears unnecessary. MR imaging may give relevant additional information and should be used as a tertiary method in patients with mammographically dense breasts, or inhomogeneous tissue on sonography, or both. More and larger studies with whole-breast sonography are necessary to confirm our findings, and long-term observation periods are needed to determine the possible influence of imaging on the incidence of recurrence in and on the overall prognosis of patients with breast cancer.
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