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Breast Imaging |
1 Department of Diagnostic Imaging, Istituto Policlinico San Donato, Via Morandi
30, San Donato Milanese, Milan 20097, Italy.
2 Institute of Radiology, University of Ancona, Via Conca, Ancona 60020,
Italy.
3 Department of Radiology, Vita-Salute University, San Raffaele Hospital, Via
Olgettina 60, Milan 20132, Italy.
4 Institute of Radiology, Udine University, Via Colugna 50, Udine 33100,
Italy.
5 Department of Diagnostic Imaging and Interventional Radiology, University of
Tor Vergata, Viale Oxford 81, Rome 00133, Italy.
6 Department of Senology, Policlinico Universitario, Piazza G. Cesare 11, Bari
70124, Italy.
Received August 14, 2003;
accepted after revision March 23, 2004.
The Italian Trial for Breast MR in Multifocal/Multicentric Cancer was
promoted by the Italian Association for Medical Radiology (Sections of
Senology and Magnetic Resonance) and supported by Bracco Imaging SpA.
Abstract
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SUBJECTS AND METHODS. Ninety patients with planned mastectomies (nine bilateral) underwent mammography and dynamic gadolinium-enhanced MRI. Off-site reviewers aware of the entry criterion (planned mastectomy) evaluated both examinations for the presence of malignant foci, recording the density pattern on mammography. The gold standard was pathologic examination of the whole excised breast (slice thickness, 5 mm).
RESULTS. Of 99 breasts, pathologic findings revealed 52 unifocal, 29 multifocal, and 18 multicentric cancers for a total of 188 malignant foci (158 invasive and 30 in situ). Overall sensitivity was 66% (124/188) for mammography and 81% (152/188) for MRI (p < 0.001); 72% (113/158) and 89% (140/158) for invasive foci (p < 0.001); and 37% (11/30) and 40% (12/30) for in situ foci (p > 0.05, not significant), respectively. Mammography and MRI missed 64 and 36 malignant foci, respectively, with median diameters of 8 and 5 mm (p = 0.033) and an invasive–noninvasive ratio of 2.4:1 (45:19) and 1.0:1 (18:18) (p = 0.043), respectively. The overall positive predictive value (PPV) was 76% (124/164) for mammography and 68% (152/222) for MRI (not significant). In breasts with an almost entirely fatty pattern, sensitivity was 75% for mammography and 80% for MRI (not significant), and the PPV was 73% and 65% (not significant), respectively. In breasts with fibroglandular or dense pattern, the sensitivity was 60% and 81% (p < 0.001), and the PPV was 78% and 71% (not significant), respectively.
CONCLUSION. MRI was more sensitive than mammography for the detection of multiple malignant foci in fibroglandular or dense breasts. Mammography missed larger and more invasive cancer foci than MRI. A relatively low PPV was a problem for both techniques.
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5 cm) or multicentricity (> 5 cm). Relapses after conservative
surgery are frequently due to undetected malignant foci
[1,
5]. The sensitivity of mammography for detecting multiple malignant foci frequently depends on the setting but is often less than 50% [5–11]. With gadolinium-enhanced dynamic MRI, sensitivities of 94–99% for invasive cancers and 50–80% for in situ cancers have been reported [7, 12–17], whereas specificities of approximately 65–79% have been obtained when integrating morphologic and dynamic criteria [16, 18]. Several reports have unequivocally shown the higher sensitivity of MRI compared with that of mammography for the detection of multifocal, multicentric breast cancer [2, 5, 7–9, 11, 16, 19–21]. In these reports, patient treatment was changed in 11–18% of the cases [7, 16, 22, 23]. Typically, MRI and mammographic findings in the previously mentioned studies were compared with a pathologic gold standard involving the suspected areas in each breast. Unfortunately, the whole breast was rarely considered, resulting in an underestimation of the false-negative findings with both techniques.
Generally, only a few reports are available on the importance of the whole-breast pattern for the diagnosis of multifocal, multicentric breast cancer [11, 16, 24]. The aim of our study was therefore to compare mammography and MRI for the detection and diagnosis of multiple breast cancer foci in potential candidates for mastectomy using the whole-breast pathologic examination as a gold standard.
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Patients
Patients who were 18 years old or older of any race, with proven breast
cancer and a planned mastectomy (proposed by the surgeon or oncologist or both
or based on the patient's preference) were eligible for recruitment. Exclusion
criteria were absolute contraindications to MRI, pregnancy or breast feeding,
severe renal failure, known hypersensitivity to gadolinium chelates, inclusion
in other clinical trials during the month before enrollment, and clinical
status that would limit data reliability. The study was approved by the ethics
committee of each center. Patients gave informed written consent to the
protocol and to the use of the data obtained from statistical analysis for
publication. A total of 153 patients were enrolled, with a mean ± SD of
9 ± 7.8 patients at each center (range, 1–32; median, 7).
Imaging Methods
Mammography was performed with standard high-quality methods involving two-
or three-view examinations, using additional projections or targeted
compression and magnification when required.
Dynamic MRI was performed on days 7–14 of the menstrual cycle in premenopausal women but without scheduling limitations in postmenopausal women. A long-line cubital or hand venous access was obtained before starting the examination. Precontrast images were acquired using a 3D spoiled gradient-echo coronal sequence. The sequence parameters were as follows: TR range/TE range, 12–18.5/1.7–7 (chosen to avoid phase opposition between fat and water, depending on the field strength); flip angle, 25–45°; 50% rectangular field of view, from 16 x 32 cm to 20 x 40 cm; and matrix, from 93 x 256 to 230 x 256 (in-plane spatial resolution from 0.7 x 1.3 mm to 2.2 x 1.6 mm). A slice thickness of 3 mm or less with no interslice gap covered both breasts. The overall acquisition time ranged between 84 and 90 sec.
An IV bolus injection of gadoteridol (Pro-Hance, Bracco Imaging SpA) was given at a standard single dose of 0.1 mmol/kg and at a rate of 2 mL/sec. This was followed by a flush of 20 mL of saline solution at the same rate. Injection of contrast agent and saline flush was performed using an automatic injector.
The postcontrast MRI sequence was identical to the precontrast sequence. The former was acquired beginning 12 sec after initiation of the contrast injection and was repeated with a temporal resolution of 90 sec or less, up to 8 min after injection. The 12-sec delay ensured that the contrast agent reached the breast when the central k-space lines (with image-contrast information) were acquired.
Postprocessing involved temporal subtraction (postcontrast minus precontrast), the acquisition of maximum intensity projections and multiplanar reconstructions, and the construction of dynamic signal intensity–time or percentage enhancement–time curves or both for regions of interest (3 x 3 pixels) positioned within the suspected lesion on subjectively determined areas of maximal enhancement.
Pathologic Examination
Pathologic examinations were performed onsite and covered the entire
excised breast. Slices of 5 mm were acquired after a consensus meeting of
pathologists from each center. Breast lesions were located using a nine-region
map (eight segments plus the nipple region) and were diagnosed according to
the 1981 World Health Organization breast cancer classification
[26].
Off-Site Image Evaluation and Radiologic–Pathologic Correlation
All mammographic, MRI, and pathologic data were collected and processed by
a central unit. The off-site reviewing of mammograms and MR images was
performed by two experienced radiologists in consensus. The reviewers were
aware of the entry criterion (planned mastectomy) but were blinded to all
patient data and to the results of the pathologic examination. A diagnostic
score from 1 to 5 (1, negative; 2, benign; 3, probably benign; 4, suspicious;
and 5, highly suggestive of malignancy) was assigned to each mammographic or
MRI finding. For MRI, morphologic and dynamic data (initial signal-intensity
increase, post-initial-signal behavior, shape, border, and contrast agent
distribution within enhancing tumors) were combined according to the criteria
defined by Fischer et al. [16]
and reported by Baum et al.
[27]. Scores of 1–3
according to Baum's classification were considered negative, whereas scores of
4–8 were considered positive. The classification method is explained in
detail in Appendix 1. The
density pattern on mammography was recorded as almost entirely fatty,
scattered fibroglandular or heterogeneously dense, or extremely dense.
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Comparison of the location of the breast foci at pathologic examination, on mammography, and on MRI was performed off-site using the same nine-region map. A third radiologist matched mammographic and MRI findings and pathologic reports. Care was taken during the lesion-matching procedure to account for vertical displacement in the oblique projection on mammograms and to consider all available MRI data (subtracted scans, maximum intensity projections, and multiplanar reconstructions). The database obtained from the lesion-matching procedure permitted analysis on both a lesion-by-lesion basis and a breast-by-breast basis.
On the basis of the pathologic report, unifocal cancer was indicated when only one malignant focus was found in the breast, multifocal cancer was indicated when more than one malignant focus was shown in the same or in contiguous segments of the nine-region map, and multicentric cancer was indicated when noncontiguous regions were involved.
Quality Check
A number of patients among the 153 enrolled patients were not eligible for
evaluation. A total of 42 patients were excluded because mastectomy was
ultimately not performed (some patients opted for presurgical adjuvant
chemotherapy), resulting in the absence of a pathologic gold standard for the
entire breast or because the mammography, MRI, or pathologic examinations were
either incomplete or subject to imaging artifacts (e.g., patient movement
between the pre- and postcontrast MRI). An additional 21 patients were
excluded from analysis at the central off-site unit because of protocol
violations during MR image acquisition (e.g., a slice thickness of 4 mm rather
than 3 mm in patients with large breasts). No exclusion from data analysis was
due to the results of mammography or MRI.
Ninety patients (58.6 ± 16.1 years old) with complete mammographic, MRI, and pathologic correlation were therefore available for evaluation. This population included nine bilateral synchronous breast cancers to give a total of 99 breasts for subsequent statistical analysis.
Focus-by-Focus Analysis
The focus-by-focus analysis comprised determinations of the sensitivity and
positive predictive value (PPV) of MRI compared with those of mammography for
the overall population and for the fatty, scattered fibroglandular or
heterogeneously dense, and extremely dense breast subgroups. Specificity was
not calculated because neither mammography nor MRI was aimed at detecting
benign lesions. The malignant foci missed with both techniques were
pathologically classified as either invasive or noninvasive for calculation of
an invasive–noninvasive ratio. A comparison of the dimensions of foci
missed on mammography with those missed on MRI was performed. Finally,
sensitivities for the detection of invasive and in situ foci were
calculated.
Breast-by-Breast Analysis
For the breast-by-breast evaluation, understaging was defined as occurring
when a malignant focus of 1 or greater was missed on mammography or MRI,
correct staging was defined as occurring when mammography or MRI detected the
exact number of foci according to the nine-region location of malignant foci
revealed at pathology, and overstaging was defined as occurring when one
false-positive focus of 1 or greater was present on mammography or MRI.
Statistical Analysis
Nonparametric McNemar, Mann-Whitney U, and chi-square tests were
used.
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The pathologic type of foci missed on mammography and MRI is reported in Table 3, whereas the numbers of concordant and discordant cases for mammography versus MRI for the 188 malignant foci are reported in Table 4.
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Overall, the global sensitivity for detection was 66% (124/188) for mammography and 81% (152/188) for MRI (p < 0.001, McNemar test). The sensitivity was 72% (113/158) and 89% (140/158), respectively (p < 0.001, McNemar test), for the detection of invasive foci and 37% (11/30) and 40% (12/30), respectively (p > 0.05 [not significant], McNemar test), for the detection of in situ foci. Mammography missed a total of 64 malignant foci compared with a total of 36 malignant foci missed on MRI. The median diameters of the missed malignant foci were 8 and 5 mm, respectively (p = 0.033, Mann-Whitney U test). The invasive–noninvasive ratio of missed lesions was of 2.4:1 (45:19) on mammography compared with 1.0:1 (18:18) on MRI (p = 0.043, chi-square test). The global PPV was 76% (124/164) for mammography and 68% (152/222) for MRI (p > 0.05 [not significant], chi-square test).
The sensitivity and PPV of both techniques for the subgroups of breast pattern together with statistical comparisons are reported in Table 5. In breasts with a fatty pattern, the sensitivity for detection was 75% for mammography and 80% for MRI (p > 0.05 [not significant], McNemar test). Likewise, the PPV was 73% on mammography and 65% on MRI (p > 0.05 [not significant], chi-square test). For the remaining breast pattern subgroups considered together, the sensitivity for detection was 60% for mammography and 81% for MRI (p < 0.001, McNemar test), whereas the PPV was 78% and 71% (p > 0.05 [not significant], chi-square test), respectively. Examples comparing MRI with mammography are given in Figures 1A, 1B, 1C, 1D, 2A, 2B, 2C, 2D, and 2E.
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The diagnostic performance in terms of understaging, correct staging, and overstaging on a breast-by-breast basis are reported in Table 6. Both mammography and MRI detected all nine cases of synchronous bilateral cancer.
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Physical examination, mammography, and fine-needle aspiration cytology are known to be inadequate solutions to this problem, as shown recently by Drew et al. [9]. The contribution of sonography may also be important [32]. However, MRI has recently been shown to be more sensitive than a combination of mammography and sonography for the detection of multiple breast cancer foci [11].
To our knowledge, this is the first large study in which a whole-breast pathologic examination was used as a gold standard for defining the diagnostic performance of mammography and MRI in looking for multifocal, multicentric disease. The number of malignant foci was approximately 1.9:1 (188:99) per breast overall and 2.9:1 per breast if only the 29 multifocal and 18 multicentric cancers are considered in the absence of the 52 unifocal cancers.
In our setting, mammography achieved an overall sensitivity of 66% for the detection of malignant foci. This value is higher than that previously reported [5–11]. On the other hand, there was a trade-off in terms of false-positive lesions because a total of 40 false-positive lesions were determined on mammography for a PPV of 76%. Although this number was higher than the 68% obtained for MRI, the results were not significantly different. In terms of multifocal, multicentric cancers, false-positive results were a clear problem for both techniques. A PPV of 76% for mammography may be considered a striking performance, but this can be attributed in large part to the selection of potential candidates for mastectomy with almost two (1.9) malignant foci per breast, of whom 47% had multifocal, multicentric cancer.
MRI was certainly better than mammography for the detection of multiple malignant foci in our series. However, 19% of the malignant foci remained undetected on MRI. This may have been a result of insufficient spatial resolution, as suggested by the dimensions of the missed foci (median diameter of missed foci on MRI, 5 mm; median diameter of detected foci on MRI, 8 mm). Alternatively, the missed cancers may have had a low level of angiogenesis.
MRI achieved a sensitivity of 89% for the detection of invasive foci, a 17% gain over mammography (72%). However, the sensitivity for the detection of in situ foci was only 40%, which was comparable to the 37% achieved with mammography. The difference between our MRI sensitivities for both invasive and noninvasive cancers and those generally reported in the literature (94–99% and 50–80%, respectively) is probably due to the more accurate gold standard in our study (whole-breast pathologic examination). This advantage is found in particular for in situ cancers on both mammography and MRI because these cancers can often be recognized only serendipitously at pathology. The ability to recognize microcalcifications on mammography does not offer a real gain in sensitivity in comparison with MRI.
Our results were expected. Hlawatsch et al. [11] reported a sensitivity on MRI of 81% for the correct diagnosis of multifocal, multicentric cancer compared with that of mammography alone (48%) and with a combination of mammography and sonography (63%). Similarly, Malur et al. [17] reported a sensitivity of only 26% for the detection of multifocal cancers on combined mammography and sonography compared with 67% on MRI. The sensitivities for the detection of multicentric cancers were 56% and 89%, respectively [17]. Fischer et al. [16] reported a sensitivity of only 58% on MRI for the detection of in situ cancers. The higher sensitivity of mammography (86%) and MRI (93%) reported by Fischer et al. in their large series of 405 malignant lesions in 336 patients was probably due to the lower overall prevalence of multifocal, multicentric cancers (1.2 malignant lesions per patient compared with 1.9 in our series).
The invasive–noninvasive ratio of our missed lesions with mammography was 2.4:1 versus 1.0:1 for MRI. These data enhance dramatically the difference in sensitivity between the two techniques. Interestingly, combining mammography and MRI achieved a sensitivity of only 83% (156/188 detected lesions) because of the presence of only three lesions that were false-negative on MRI and true-positive on mammography.
Despite the fact that MRI is the best technique available for the detection of multifocal, multicentric breast cancers, improved performance may still be achievable. In terms of sensitivity, a gain could be achieved using a higher in-plane and through-plane spatial resolution. In terms of specificity, improved performance may be achieved by integrating the best morphologic and dynamic data [26], by means of proton MR spectroscopy [33], and by the use of short-term antiestrogen (tamoxifen) medication before MRI [34].
As indicated previously, the PPV of 68% for MRI was not significantly different from that of mammography. This well-known problem makes the availability of MRI-guided biopsy mandatory for centers that intend to use MRI as a diagnostic staging tool.
The analyses of mammographic patterns to give indications for clinical practice. The difference in sensitivity between mammography and MRI was not significant in breasts with a fatty pattern but was largely significant in nonfatty breasts. MRI sensitivity, on the other hand, was not influenced by the density of the breast, and the PPV does not depend on breast pattern. In patients with a nonfatty pattern and at least one suspicious lesion on mammography, sonography could be performed after and not before MRI. Thus, the first and the second sonographic examinations could be combined to exploit the good sonographic sensitivity for multifocal, multicentric breast cancer [11, 32] and to recognize (with immediate biopsy) a large number of the foci detected on MRI [35]. Our results confirm those of Hlawatsch et al. [11], who used a score density of 1–5 and showed treatment-relevant additional information on MRI in patients with a mean score of 4.0.
The results of the breast-by-breast analysis can also be considered to have been influenced by the whole-breast gold standard. Both mammography and MRI correctly staged only 51% of the breasts, whereas a mirrorlike pattern of understaging and overstaging was noted for the remaining breasts: 30% and 19%, respectively, for mammography; and 19% and 30%, respectively, for MRI. These results indicate that understaging of 30% of breast tumors would have occurred on mammography alone, whereas in 19% of the cases, biopsy under stereotactic guidance would have been indicated. Conversely, on MRI, 19% of breast tumors would have been understaged, whereas 30% would have undergone biopsy under MRI guidance. Practically, these results suggest that MRI may give more information if a second conventional evaluation is performed (e.g., a second mammography to acquire new tailored views or magnifications or a targeted sonography after MRI). Moreover, MRI-guided biopsy should be performed only when MRI-detected foci remain undefined.
Synchronous bilateral breast cancer affects approximately 10% of our potential candidates for mastectomy. All the bilateral cancers in our series were found with both techniques. Unlike reviewers in other studies, the mammography reviewers in our study were aware that both breasts were candidates for mastectomy. In the study by Fischer et al. [16], additional contralateral carcinomas were depicted on MRI alone in just 79% (15/19) of the cases. Without MRI and using a clinical reviewing setting for mammography, a substantial number of bilateral breast cancers would have been missed with the result that the undetected contralateral focus would have been untreated.
In conclusion, starting from the viewpoint that conservative therapy for breast cancer requires the ability to screen the entire breast for additional sites of malignancy with a high sensitivity (a difficult task in dense breasts), we compared MRI to mammography in breasts of various densities. Our results indicate that MRI is significantly more sensitive than mammography for the detection of multiple malignant foci in scattered fibroglandular or heterogeneously and extremely dense breasts, but is not significantly more sensitive in fatty breasts. Mammography misses more invasive and larger cancer foci than MRI. However, false-positives are a problem for both techniques. The relatively low specificity of MRI makes the availability of MRI-guided breast biopsy mandatory. Despite the extra cost involved in introducing MRI into the diagnostic workup of breast cancer, the conclusion of Essermann et al. [2] that MRI "would be valuable as a staging tool in the preoperative setting even if the cost is in the range of $1,300 to $2,000" should be considered.
We are aware that the real clinical significance of malignant foci detected solely on MRI is still a matter for debate [36]. If combined with radiation therapy, breast-conserving surgery gives survival rates that are not significantly different from those obtained with mastectomy [31, 37]. Randomized studies comparing the outcome of patients undergoing pretreatment MRI with a control group not undergoing pretreatment MRI are needed to define the effects of a more precise evaluation of the extent of disease on relapse rate, quality of life, and survival rate. One such trial has just begun in the United Kingdom [36]. However, until the results of this or other similar studies become available, we suggest a dynamic MRI examination before treatment planning in patients with a nonfatty breast pattern.
Acknowledgments
The Italian Trial for Breast MR in Multifocal/Multicentric Cancer was
promoted by the Italian Association for Medical Radiology (Sections of
Senology and Magnetic Resonance) and supported by Bracco Imaging Spa.
Enrolling centers were Ferrara, Ospedale S. Anna (S. Corcione); Ancona,
University, Ospedale Torrette (G. M. Giuseppetti); S. Giovanni Rotondo,
Scientific Institute (M. Cammisa) and Chieti, University (L. Bonomo); Aviano,
Centro di Riferimento Oncologico (S. Morassut); Udine, University, Policlinico
(M. Bazzocchi); Trieste, University, Ospedale Gattinara (R. Pozzi Mucelli);
Siena, University, Policlinico Le Scotte (P. Stefani); Rome, Ospedale
Fatebenefratelli (A. Orlacchio); Milan, European Institute of Oncology (M.
Bellomi); Milan, Vita-Salute University, Ospedale S. Raffaele (P. Panizza);
Milan, Istituto Nazionale Tumori (R. Musumeci); Rome, Tor Vergata University
(G. Simonetti); Firenze, University, Ospedale Careggi (N. Villari) and Center
for Study and Prevention of Cancer (D. Morrone); Reggio Emilia, Ospedale (A.
Troiso); Genoa, University, Ospedale S. Martino (F. Sardanelli, now at
Istituto Policlinico San Donato, San Donato Milanese, Milan, Italy); L'Aquila,
University, Ospedale S. Maria (G. Masciocchi); Como, Ospedale S. Anna (G.
Gozzi); Milan, Ospedale S. Carlo (D. Vergnaghi); and Modena, University,
Policlinico (R. Romagnoli).
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