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Institutes of 1 Diagnostic and Interventional Radiology, and 4 Gynecology Friedrich-Schiller-University, Bachstrasse 18, D-07740 Jena, Germany, 2 Shao Yi Fu Hospital, Medical College of Zhejiang University, Qingchun East Road 3, Hangzhou 310016, P. R. China and 3 Institute of Pathology, Friedrich-Schiller-University, Ziegelmuehlenweg 1, D-07747 Jena, Germany
Correspondence: Henning Neubauer, c/o Li Mengxia, Department of Paediatrics, Shao Yi Fu Hospital, Qing Chun Dong Lu 3, Hangzhou 310016, P.R. China
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Introduction |
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With recent advances in mammographic techniques and interpretation, the percentage of DCIS accounting for all newly diagnosed breast cancers has increased from approximately 1% to 15–25% [2, 3]. Due to progress in imaging, a typical case of DCIS these days is small (1–2 cm), non-palpable and detected on mammography.
DCIS is considered a possible precursor of invasive carcinoma of the breast. It has become evident over time that DCISs are a highly heterogeneous group of tumours. Thus a more differentiated approach to imaging and therapy of DCIS seems desirable [4]. A multitude of investigations on the biological, genetic and histopathological characteristics of DCIS revealed a vast range of possible expression of significant biochemical markers such as oestrogen and progesterone receptors, c-erbl, Ki-67, PCN and Cathepsin E. Those findings correlate well with striking differences in cytological and histological features as well as in the biological potential [5–8]. A variety of schemes have been developed for the histopathological classification of DCIS, including the classification introduced by Holland [9] and the van Nuys classification system [10].
Dynamic MR mammography (MRM) has become a well established method in the diagnosis of invasive breast cancer, with a sensitivity approaching 100% [11–15]. Experience with DCIS on dynamic MRM, however, is still limited. Review articles that describe the typical appearance of DCIS on MRM have recently been published [16–18], and yet, the typical features of DCIS on MRM are still not well characterized. All previous studies were performed on small groups of patients [19–23]. Only one study compared DCISs of different gradings [23] and only one study included pure DCISs only [20]. Most DCISs seem to enhance on MRM. A major percentage of DCISs, however, cannot be distinguished from benign breast disease. A wide range of sensitivities (43–96%) were reported with a similarly wide range of MRM parameters and different criteria for malignancy used. In the literature, there is no consensus on the value of MRM in the diagnosis of DCIS.
The typical kinetics of signal increase and the characteristic pattern of enhancement morphology for pure DCIS were studied. Furthermore, differentiation between high grade and non-high grade DCIS with regard to the van Nuys classification was attempted. The hypothesis of different MR mammographic features between high grade and non-high grade DCIS was tested. With the increasing awareness of DCISs as a highly heterogeneous group of tumours, a differentiated approach to MR mammographic imaging of DCIS seems necessary and of both theoretical and clinical importance.
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Materials and methods |
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In order to measure tumour size on histological sections, areas showing growth of DCIS were defined by the pathologist. The diameter of those areas was measured in all sections and the biggest diameter referred to as the size of the DCIS lesion. Where only a single duct was affected by DCIS growth, the size of the single focus was measured as the size of the DCIS. 21 of 39 DCIS cases were located in the right breast, while 18 DCIS cases were identified in the left breast. Multifocal disease was described in 15 cases.
Patients age ranged from 25 years to 79 years, (mean 56.5 years). Seven patients presented with subjective symptoms, such as a mass discovered by the patient herself (five cases), pain (one case) and eczema of the nipple (one case). On physical examination, a palpable mass was found in 18 (46%) patients. One patient was suspected to have Paget's disease of the nipple. Two patients had a history of invasive breast cancer of the contralateral breast. Six patients were on hormone replacement therapy at the time of MRI examination, one patient had discontinued hormone therapy three weeks prior to MRM. 22 patients were post-menopausal and one had undergone hysterectomy. The remaining patients were examined in the first half of the menstrual cycle, except for three patients who underwent MRM on the 21st, 21st and 24th day of their respective cycles.
34 of 39 patients had mammography prior to MRM at our institute. Two patients had mammography at another hospital. 36 patients had breast ultrasound following mammography, while two patients of 25 years and 33 years of age, were examined with breast ultrasound only. One patient with a papable mass was examined with MRM only. Mammography showed microcalcifications in 21 of 36 patients, densities suspicious for malignancy in 7 cases, densities and microcalcification together in 1 case and otherwise unclear but suspicious findings in 2 cases. In four patients there were no suspicious findings on mammography. Breast ultrasound was considered suspicious for malignancy in 24 of 38 patients.
All MRM examinations were performed on a 1.5 T unit (Gyroscan S15 ACS II; Philips Medical Systems, Hamburg, Germany) according to the same examination protocol. A dedicated double-breast surface coil was used and bilateral scans obtained. Before examination, a needle for the intravenous administration of contrast agent was placed in a cubital vein and the patient put in a comfortable prone position.
The MR examination was performed in five steps: (1) a localizer sequence (T1 weighted spin echo 121 ms repetition time (TR), 13 ms echo time (TE), 90° flip angle, slice thickness 5 mm, field of view 450); (2) a two-dimensional (2D) gradient echo sequence to plan the dynamic sequence, and (3) the dynamic 2D fast field echo (FFE) sequence (96 ms TR, 5.0 ms TE, 80° flip angle) was then acquired. One series consisted of 24 transverse sections with a slice thickness of 4 mm, a matrix of 256 x 256 pixels and a field of view of 350 mm. After initial aquisition without contrast agent, a bolus of 0.1 mmol kg-1 gadolinium-DTPA (Gd-DTPA) (Magnevist®; Schering, Berlin, Germany) was administered intravenously without moving the patient, followed by an injection of saline. Following this, seven sets of dynamic images were recorded, each acquisition lasting 60 s. (4) Another sequence according to step (2) was then performed as post-contrast images; and (5) a set of T2 weighted images was obtained (SE, 4000 ms TR, 300 ms TE, flip angle 90°, slice thickness 4 mm).
Three independent observers, two MRM specialists and one MRM-trained resident, retrospectively evaluated the images in the course of this study. The observers were aware of the diagnosis of DCIS, but they did not know the side, location or size of the tumour. Sets of substraction images computed from the dynamic series were the basis for evaluation. PC software was used to determine the regions of interest (ROIs) in areas of colour-encoded signal increase. Suspicious lesions were evaluated by the repeated determination of small ROIs of 2 x 2 and 3 x 3 pixels, looking for the most enhancing part of the tumour.
Criteria for suspicious signal increase were defined corresponding to those commonly used for invasive carcinoma. A relative signal increase of at least 90% in the first or second minute followed by a plateau or washout phenomenon were considered suspicious for malignancy. Distinct categories of signal enhancement (Figure 1
, Figure 2a–d) and morphological patterns (M0–M4) were defined to ensure a higher objectivity and better inter-observer reliability (Figure 2e–g, Figure 3). The course of signal enhancement was described as normal (C1), slow-continuous (C2), strong initial and slow further increase (C3), strong initial increase followed by a plateau phenomenon (C4) and strong initial increase followed by a washout phenomenon (C5). The morphological pattern categories included: no pattern observed (M0); linear or linear-branched (M1); segmental dotted or granular (M2); segmental homogeneous (M3); and focal spot-like enhancement (M4). As the study design was not clinical and the main objective was to identify characteristic MR mammographic features of DCIS in a group of known DCIS patients, it was decided that the term "sensitivity" be avoided and "rate of detection" be used instead.
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Results |
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). Strong early signal increase (C3–C5) was observed in 10 of 12 (83.3%) high grade DCISs and in 11 of 12 (91.7%) G2 DCISs. Of the 27 non-high grade DCIS, only 33.3% showed a plateau phenomenon and 18.5% showed a washout phenomenon. In this group, 74.1% of tumours were found to have a strong initial signal increase (C3–C5). 6 (40.0%) of the 15 G1 DCISs did not show any enhancement.
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Evaluation 1), with a rate for G1, G2 and G3 of 40.0%, 66.7% and 83.3%, respectively.
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). A similar segmental enhancement, but with a homogeneous pattern (M3) was found in three (9.1%) patients. Thus, segmental enhancement was seen in 82.5% of enhancing tumours in this study, and was the most frequently observed single feature. The spot-like pattern, M4, was found in 18.2% of enhancing tumours. There was no case with an M1 pattern resembling a linear or linear-branched (ductal) enhancement.
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Evaluation 2), with a rate for G1, G2 and G3 of 53.3%, 91.7% and 91.7%, respectively. Therefore with combined evaluation, the same rate of detection for G2 and G3 lesions was reached.
Statistical tests
When enhancement kinetics only were considered Fisher's exact test failed to prove a significant difference between high grade and non-high grade DCISs (p=0.063) (Table 4, Evaluation 1). The differences in rate of suspicious signal enhancement of G1 vs G3, and G1 vs G2 and G3 grouped together, however, were found to be significant (p<0.05). No significance existed between G1 and G2, nor between G2 and G3.
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Evaluation 2). The difference between G1 and G2 tumours reached significance. Thus, with combined evaluation of enhancement kinetics and morphology, we were able to find G2 and G3 DCISs with a detection rate as high as 91.7%, a rate that was significantly higher than that for G1 DCISs (53.3%). Differences in the frequency of morphological pattern between DCIS of different grading did not show statistical significance.
Spearman's Rank correlation showed a moderate but significant correlation between tumour grade and category of signal enhancement (Spearman's Rank correlation coefficient r=0.36, p<0.05).
Median tumour size on histology was 12 mm and differed between groups of high grade and non-high grade lesions; 6 mm for G1 DCISs (range 2–15 mm), 15 mm for G2 (range 3–32 mm), and 17.5 mm for G3 (range 4–40 mm). The Independent sample T-test showed the differences between all groups to be significant, except that between G2 and G3 DCISs (Table 5). Spearman's Rank correlation showed a highly significant correlation between tumour grade and size (r=0.58, p<0.001).
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Breast ultrasound was false negative in 11 patients. In nine of these patients, MRM was suspicious. In seven patients with negative MRM, malignant disease was suspected on breast ultrasound. In particular, ultrasound found five of the six small G1 DCISs, which did not show contrast enhancement on MRM.
Two DCISs were seen on mammography alone, and a further two cases were positive on breast ultrasound only.
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Discussion |
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Whilst it is not the procedure of choice, MRM is the most sensitive method for imaging of invasive breast carcinoma with a sensitivity approaching 100% [11–15]. Investigations focusing on the MR mammographic appearance of DCIS, however, are few, ranging in sample size from 19 to 71 patients [19–23] with up to one-third of those patients having microinvasive tumours [21, 23]. Only one of those studies solely contained pure DCIS (n=35) [14]. The reported examination protocols showed a wide range of variation in terms of MR sequence, time and spatial resolution, type and concentration of contrast agent, and criteria for malignancy. Consequently, results differed considerably between these studies and sensitivities range from 43% to nearly 100%. Differences for comedo and non-comedo DCISs were reported in passing. Histological grading of DCIS lesions is known to be one of the important prognostic markers [25, 26]. Furthermore, histological grading and biochemical and genetic qualities of the tumour, which are thought to play a key role in determinating a lesion's biological behaviour, were reported to be highly correlated [5–8]. However, only one MRM study published to date looked for significant differences between high grade and non-high grade DCISs, and did not find any [23]. Much of our present knowledge regarding DCISs and their appearance on MRM is still fragmentary, preliminary and based on limited data and experience only.
Empirical observations made during routine MRM examinations at our institute suggested certain patterns of enhancement to be characteristic of DCIS. High grade lesions seemed to be more frequently associated with highly suspicious signal enhancement similar to most cases of invasive breast carcinoma. Conversely, non-high grade DCIS showed this malignant signal increase less often. DCIS also seemed to have a characteristic morphology, since a segmental enhancement, typically with a granular or dotted pattern, was thought to be frequently associated with DCIS on MRM. We undertook to verify those hypotheses in an effort of hypothesis-driven research.
Three observers independently evaluated MR images in this study, and assigned patients to the corresponding category of signal enhancement and morphology. As each category was intended to be as distinct and unequivocal as possible, inter-observer reliability in this study was good. There was unanimous agreement on the categories of signal enhancement. Only minor differences occurred in the assessment of morphology, when the decision on whether segmental enhancement was homogeneous (M3) or strongly dotted (M2) had to be made. The three observers agreed on more than 95% of their initial evaluations.
The main objective of this study was to identify and describe characteric MR mammographic features of DCIS. Therefore, and as this study was performed on a highly selected group of known DCIS patients with only partially blinded readers, the term "sensitivity" was avoided as it may suggest a clinical setting with blinded observers and control patients, and the term "rate of detection" was used instead.
Recent publications on DCIS and MRM tend to emphasize the analysis of morphological pattern, as the evaluation of signal increase alone apparently did not reach a high diagnostic sensitivity and specificity [16–18, 27]. A multitude of different terms for, and categories of, enhancement morphology have been proposed. Some of these describe the outer shape of the lesion and the relation to the adjacent normal breast tissue and some analyse the predominating pattern or the distribution of enhancement within the areas of signal increase. Similarly, a variety of categories for enhancement kinetics with different thresholds and curves of signal increase have been used. With the categories used here, we tried not to contribute to linguistic and terminological confusion and focused on patterns that are characteristic and frequently observed in daily practice and that can be applied in clinical routine on MRM with a large field of view and a relatively low spatial resolution. Categories of enhancement morphology similar to those used have been previously reported but, so far, the particular role of a unilateral segmental pattern for DCIS has not been pointed out.
Morphology
We found unilateral segmental enhancement to be the most commonly seen and most striking feature of DCIS (82%), usually combined with a granular dotted pattern, M2, (73%). This pattern seems to be typical for DCIS, with hormone effects as the only major differential diagnosis. Hormone replacement therapy is known to stimulate breast tissue in a way that intermediate signal enhancement and an M2 pattern may result. Hormone effects on MRM have been shown to be bilateral, symmetrical and synchronous with a segmental granular pattern, and to be reversible once hormone intake is stopped [28, 29]. Furthermore, no plateau or washout phenomenon were reported in relation to hormone effects [28, 29], nor in enhancing foci of healthy pre-menopausal women [30]. In our study, 61% of enhancing DCISs showed unilateral segmental enhancement in combination with a plateau or washout effect (C4, C5). In another 21% of patients, the same unilateral segmental enhancement was seen together with a strong initial (C3) or slow, continuous signal increase (C2). In all six patients undergoing hormone replacement therapy at the time of MRM examination, enhancement possibly owing to hormone effects and histologically confirmed DCIS were clearly distinguishable, as observed enhancement was either unilateral or obviously asymmetrical and not synchronous in both breasts. Therefore we suggest that, in a clinical setting, DCIS may be considered in any case of unilateral or asymmetrical segmental enhancement on MRM when intraductal disease is suspected. In addition, we support the recommendation that hormone intake should be discontinued 3 months prior to MRM if possible [28, 29]. As a result of this study and earlier experiences, we strongly recommend bilateral, simultaneous MR scans as the one means to assess and compare contrast enhancement in both breasts.
The M4 pattern was observed in six (18%) enhancing tumours. It represents a focal, spot-like pattern corresponding to a circumscribed tumour mass. Both invasive carcinomas and benign tumours, such as small fibroadenomas are known to show this pattern. The M4 pattern together with a suspicious signal increase (C4, C5) was seen in three of these six cases. Another DCIS in this category showed a strong initial signal increase (C3) and two tumours had slow, continuous enhancement. One of the latter was a 1 cm G3 DCIS that could not be correctly diagnosed as suspicious on MRM. The enhancement pattern M4 thus seems to pose a major problem for diagnosis and differential diagnosis and needs further investigation.
A pattern in a linear or branched fashion (ductal enhancement according to the M1 category) was not found in this study. It has been reported in other studies with a frequency of up to 17% [22]. This difference might be merely incidental or could be the result of different MR techniques used in terms of MR sequence, temporal and spatial resolution, slice thickness, contrast agent or others.
Kinetics of signal enhancement
The evaluation of time–intensity curves is a valuable means to distinguish between benign and malignant lesions on MRM [31]. However, less than two thirds of DCISs in this study were diagnosed with suspicious time–intensity curves of signal enhancement when the threshold of 90% for strong initial signal increase and the criteria of plateau and washout, as commonly used for invasive cancer, were applied. In particular, a considerable percentage of non-high grade DCISs, presented with intermediate kinetics and could easily be mistaken for benign lesions. The signal intensity curves of high-grade DCIS seen in this study were highly suggestive of a tendency to more malignant kinetics, compared with non-high grade DCIS. The significant results from Spearman's Rank correlation support this hypothesis. As in a previously published study [23], however, no statistical significance between non-high grade and high grade DCISs could be found to prove this hypothesis (Table 3). The aspect newly discovered in the study presented here was the significant difference between the groups of G1 and G3 DCISs, as well as between the G1 DCIS and a combined group of G2 and G3. Intermediate and high histological grading was reported to be associated with an increased rate of local recurrence in DCIS [32]. Our results regarding signal enhancement of DCIS are in line with observations from earlier studies, stating that the majority of DCIS show malignant time–intensity curves, while in a considerable number of cases findings are equivocal or even mimic benign disease.
Combined analysis of enhancement kinetics and morphology
As single factors, both malignant contrast enhancement and a unilateral, segmental pattern of enhancement were found to be suggestive of DCIS in our study. combined analysis greatly improved rate of detection for both non-high grade and high grade DCIS, most dramatically in the group of G2 DCISs, where 26% more lesions could be correctly classified with combined analysis. As a result, the rate of detection for G2 reached that of G3 DCISs (91.7%), while still little more than one half (53.3%) of the G1 DCISs were found.
Of the 33 enhancing tumours, only 3 lesions (9%), one case in each group of G1, G2 and G3, were not correctly classified due to non-suspicious kinetics (C2, C3) with a focal, circumscribed pattern of enhancement (M4). With combined analysis, 91% of all enhancing tumours (signal increase >C1) in this study could therefore correctly be described as suspicious. Naturally, those 6 G1 DCISs that did not show any enhancement were also missed with combined analysis. Among those lesions, there were four very small tumours with respective diameters of 2 mm, 2 mm, 5 mm and 5 mm on histology. Considering the slice thickness of 4 mm in this study, one cannot expect a high sensitivity for such small lesions. Conversely, a 3 mm G2 DCIS, a 4 mm G1 DCIS and a 4 mm G3 DCIS with suspicious signal enhancement (C4, C5) were found. MRM with a relatively poor spatial resolution and relatively thick transverse sections therefore seems to be able to detect very small DCISs, yet with very limited sensitivity. In this study, all G2 and G3 DCISs, large and small, enhanced (>C1). Therefore normal MRM may be helpful to exclude occult high grade DCIS. None of our findings was specific for DCIS of a particular grading. As expected, grading of DCIS lesions will continue to be a histological, not radiological, diagnosis. For optimal management of DCIS on MRM, an approach is needed that considers a multitude of factors, including enhancement kinetics and morphological patterns of enhancement on MRM, a comparison between the enhancement in the left breast and the right breast, combined assessment of results obtained from MRM as well as from clinical examination, mammography and ultrasound, and the patient's history of benign and malignant breast disease [27].
Statistical significance and tumour size
At this point it seems necessary to discuss the issue of tumour size. There is no standard method for measuring DCIS size. Furthermore, there are well known practical and theoretical limitations to the accuracy with which DCIS size, and in particular that of large, branched tumours, can be determined. The tumour sizes measured for the lesions in this study are still considered to be a good approximation. G1 DCISs were found to be significantly smaller than both G2 and G3 DCISs. Almost one half of G1 DCISs did not show suspicious findings, and 40% were completely invisible on MRM. Therefore, one may suspect that differences in contrast enhancement are in fact a result of different mean tumour size, rather than being related to histological grading. In this case, a critical size for DCIS on MRM, with the parameters used in this study, could be postulated. This can be expected to lie somewhere between the 6 mm average tumour size of G1 lesions and the 15 mm average size of G2 lesions.
In general, MRM can be expected to be less sensitive for very small lesions than it is for large tumours. Therefore, it is probably not wrong to assume that tumour size has influenced the findings in this study. Yet, differences in tumour size do not explain all the differences found between DCISs of different grading. There was no significant difference in the rate of detection between non-high grade and high grade DCISs, in spite of the significantly different mean tumour sizes (Table 4) and the significant result from Spearman's Rank correlation between tumour grading and tumour size. A comprehensive multifactor analysis performed on a large group of patients may help to decide whether tumour size only, grading only, or both factors together to a varying extent, determine the MR mammographic appearance of DCIS. This issue remains open and is surely worthy of further investigation.
MRM in relation to mammography and breast ultrasound
Apart from one patient who underwent initial MRM, all other patients initially underwent mammography and/or breast ultrasound, with suspicious findings in either one or both examinations. As suspicious findings on mammography and/or breast ultrasound were the criteria according to which patients were chosen to undergo MRM, results of the three examinations cannot easily be compared. Retrospectively, the three imaging modalities appeared to be complementary. None would have found all DCIS cases, and the combinations of mammography and MRM only or ultrasound with MRM only would both have failed to detect two cases (5%) each. As a direct result of the above mentioned selection criteria, there was no tumour diagnosed on MRM alone. Breast ultrasound seemed particularly helpful in combination with MRM, as it could correctly diagnose 5 of the 6 small G1 DCISs that did not show any enhancement on MRM scans. The "sensitivities" for the three examinations (mammography 86%, ultrasound 67%, MRM 77%) in this study are biased and mutually dependent, and cannot easily be compared with results obtain from other investigations.
Limitations
The major limitations of this study are the retrospective design and small group of selected patients. As the characteristic features of DCIS on MRM are not yet well described, and only speculations exist on possible differences between pure and microinvasive DCISs on MRM, it was though desirable to study pure DCIS only. Therefore a significant number of patients with microinvasive disease were excluded. Although this study is the largest of its kind performed with pure DCIS, the limited number of patients hardly allows a comprehensive and well founded statistical analysis. Results from small studies inevitably remain descriptive in nature, as does this study. The preselection of patients in this study may also be of concern. Owing to the selection criteria of suspicious findings on mammography and/or breast ultrasound, the cases in our MRM study are confined to a subgroup of DCIS lesions that can be diagnosed on either one or both of these two imaging modalities. An extrapolation of our results towards the behaviour of MRM in a prospective study seems inappropriate at this point. The total number of MRM examinations at any given institution is still small, and there are no large groups of unselected DCIS patients examined with MRM at present. As MRM is more frequently included in clinical trails [33], and as first studies on MRM under screening conditions are being conducted [34], more data on unselected groups of DCIS patients will become available, key indicators such as sensitivity and specificity will be determined in the appropriate clinical setting and a more elaborate and reliable statistical analysis will be possible. In the meantime, this study may help create the theoretical and practical fundament on which those larger trials will have to be based.
The dynamic MR sequence in this study was acquired as bilateral scans with a large field of view, relatively thick, continuous transverse sections and a relatively low spatial resolution. Studies facilitating high resolution MRM naturally reveal more morphological detail. However, with the MR scanners presently available in daily practice, high spatial resolution with adequate temporal resolution in the dynamic series can usually be obtained for unilateral scans only. Considering that a growing number of patients of all age groups can be expected to present with hormone effects on MRM, we presently favour the evaluation of simultaneous bilateral MR scans over unilateral scans, though the latter shows a gain in spatial resolution.
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Summary |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSummaryReferences |
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Normal MRM may help to exclude high grade DCIS, a result from our study that may have an immedate impact on daily practice. Furthermore, 91.7% of the G2 and G3 DCISs could be correctly identified in this study, suggesting that MRM is a sensitive imaging method for high grade DCIS. MRM could thus play a role in post-operative follow-up and in the examination of high-risk patients when mammography and ultrasound fail to show suspicous lesions.
Pre-operative MRM can give valuable information for the planning and preparation of surgical biopsy [15]. Whilst mammography and ultrasound tend to underestimate tumour size, MRM does not show a significant difference in size compared with histological evaluation in both invasive and in situ carcinoma [36]. With the high rate of detection reported in this study, MRM appears to have the potential to contribute to the pre-operative assessment of DCIS patients.
In addition to MRM studies on a larger number of patients to verify the preliminary results presented here, further investigations are necessary to study the biochemical and histopathological features of DCIS. Once the natural course of the disease and the different biological potential of high grade and non-high grade DCIS are better understood, it will also be possible to draw more definite conclusions on the value of MRM in the diagnosis of DCIS. In the meantime, DCIS will continue to be a challenge for every radiologist working in the field of MR mammography.
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Acknowledgments |
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Received for publication August 6, 2001. Revision received September 6, 2002. Accepted for publication October 21, 2002.
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