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Breast Imaging |
1 From the Department of Radiology and Radiation Therapy, University of Bonn, Sigmund-Freud-Str 25, D-53105 Bonn, Germany. From the 1999 RSNA scientific assembly. Received February 27, 2002; revision requested May 17; final revision received April 7, 2003; accepted May 20. Address correspondence to N.M. (e-mail: n.morakkabati@uni-bonn.de).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: A total of 116 dynamic bilateral breast MR studies were performed during and up to 12 months after radiation therapy in 72 patients who had undergone breast-conservation surgery without preoperative MR imaging. Patients were assigned to four groups according to the time span between imaging and radiation therapy. Structural changes, parenchymal enhancement pattern, and prevalence and imaging features of incidental lesions were analyzed and compared with those of the nonirradiated breast.
RESULTS: Radiation therapy led to parenchymal edema and a significant (two-tailed paired Student t test) increase in enhancement rates in the irradiated compared with those in the contralateral breasts during and up to 3 months after radiation therapy. Neither during nor at any time after radiation therapy did the mean enhancement rates reach diagnostically relevant rates. Unsuspected residual or recurrent breast cancers were identified in irradiated breasts of five patients and in contralateral breasts of two patients. False-positive MR findings resulted in a biopsy in three patients with irradiated and in one patient with nonirradiated breasts. There was no difference in enhancement kinetics or morphology of benign or malignant lesions in irradiated versus nonirradiated breasts.
CONCLUSION: Radiation-induced changes occur at MR imaging during or up to 3 months after radiation therapy but are much less severe than reported. Detection and characterization of lesions were feasible with comparable diagnostic accuracies in irradiated and nonirradiated breasts.
© RSNA, 2003
Index terms: Breast, MR, 00.121412, 00.121415, 00.12143 • Breast neoplasms, therapeutic radiology • Radiations, injurious effects, 00.47
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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During the first 12–18 months after radiation therapy, however, contrast enhancement associated with radiation-induced inflammatory changes has been reported to severely impair the interpretation of breast MR images. Therefore, breast MR imaging is not indicated in the early period after radiation therapy (12,13). Yet, these recommendations stem from a time when interpretation of MR images relied on assessment of enhancement rates alone. Today, more refined diagnostic criteria are in use that improve the differentiation of contrast enhancement caused by benign from that caused by malignant lesions (14). Thus, the objectives of our study were to investigate the degree and prevalence of radiation-induced changes on breast MR images in patients who were undergoing radiation therapy at that time or soon after, to assess prospectively whether possible radiation therapy–induced effects impair the diagnostic accuracy of breast MR imaging, and to investigate the prevalence of residual ipsilateral and synchronous contralateral breast cancer as revealed at breast MR imaging in patients undergoing radiation therapy after lumpectomy or quadrantectomy for a supposedly solitary breast cancer.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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A prospective comparative combined inter- and intraindividual trial with a horizontal study design was performed in 72 consecutive women who, after having undergone breast-conserving therapy elsewhere, received radiation therapy at the authors’ institution.
Of the 72 patients, 33 consented to be examined more than once (up to three times) during the 1-year period after radiation therapy, such that a total of 116 breast MR studies were performed during the study period and were available for assessment.
Time-dependent changes in the prevalence and the extent of possible radiation therapy–induced effects were assessed intraindividually with 44 follow-up studies in 33 patients and interindividually with the inclusion of patients at four intervals (groups A–D) after radiation therapy.
Group A consisted of 44 breast MR studies in patients who were at that time undergoing radiation therapy. At the time of the study, the patients had received half of the intended dose of 60 Gy.
Group B consisted of 12 breast MR studies in patients who had undergone radiation therapy as many as 3 months earlier (nine new participants and three patients who underwent follow-up studies in group A).
Group C consisted of 30 breast MR studies in patients who had undergone radiation therapy 3–6 months earlier (11 new participants and 19 patients undergoing follow-up studies).
Group D consisted of 30 breast MR studies in patients who had undergone radiation therapy 6–12 months earlier (eight new participants and 22 patients undergoing follow-up studies).
For each group, radiation-induced changes were assessed with intraindividual comparison of the irradiated and the nonirradiated breast. This meant that for each patient and each group, the nontreated contralateral breast served as the internal reference standard for the evaluation of the extent of radiation therapy–induced effects.
Diagnostic accuracy (sensitivity, specificity, and positive and negative predictive values) of MR imaging of the irradiated breast at the four time spans during or after radiation therapy was compared with the diagnostic accuracy of the technique in the same patient’s contralateral breast. In addition, we recorded the prevalence and stage of breast cancers that were newly diagnosed during the study.
Patients
The mean age of the 72 study participants was 50.9 years (range, 31–70 years). Fourteen (19%) of the 72 patients were premenopausal. All patients had undergone breast-conserving therapy elsewhere and received radiation therapy at the authors’ institution. None of the patients had undergone a preoperative breast MR study for local staging.
The pTN stages of the patients’ primary tumors (for which they were undergoing radiation therapy) are listed in Figure 1. All patients underwent wide local excision; all specimens were subjected to extensive histologic assessment to check for free margins. In cases with tumor at or close to the surgical margin, local reexcision was performed at the time of axillary dissection to establish a tumor margin distance of 8–10 mm. With one exception, all patients had histologically confirmed clear margins at presentation for radiation therapy to our department. The one exception was a 52-year-old patient with ductal invasive cancer stage pT2N1 whose cancer was histologically known to abut one of the specimen margins. However, this patient did not exhibit residual or recurrent breast cancer during the study period or during the 2-year follow-up (recurrence was excluded on clinical grounds and mammographic, breast US, and MR imaging findings).
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Validation of MR Diagnoses
Breast MR imaging diagnoses were validated at excisional or core biopsy in cases with suspicious findings or at close clinical, mammographic, and high-frequency (10-MHz) breast US follow-up in patients with no or benign findings. We perform systematic quadrant-based and radial scanning and, because US is done in an attempt to identify additional mammographically occult ipsilateral or contralateral tumors, we would always and without exception scan both entire breasts. At the time this article was written, all patients were undergoing mammographic (every 6 months) and sonographic (every 3 months) follow-up for more than 24 months (24–48 months). In addition, a 24-month breast MR imaging follow-up was performed in 43 of the 72 patients. One patient died of distant metastases 3 years after treatment, without evidence of local recurrence. Two patients developed recurrent breast cancer 3 and 4 years after breast-conservation surgery. The recurrent tumors were both detected during routine follow-up as newly developed densities; both patients underwent MR imaging before biopsy, and the images were compared with the MR images obtained during the study period. This comparison did not reveal any signs of breast cancer at the site of recurrence. We assume that these tumors represent true recurrent cancers.
In 11 patients, suspicious lesions were identified on MR images that had no correlate on conventional images (recent mammograms or repeat targeted US scans). These lesions were clarified with MR-guided excisional or MR-guided core biopsy (15,16).
Radiation Protocol
All patients received a total dose of 60 Gy (50 Gy for the entire breast and an additional 10 Gy for the tumor bed), with a single dose of 2 Gy five times per week (Mevatron MD2; Siemens Medical Solutions, Erlangen, Germany). The mean time span between surgery and the start of radiation therapy was 9 weeks (range, 2–36 weeks; SD, 6 weeks).
Breast MR Imaging Technique
Breast MR imaging was performed with a 1.5-T system (ACS II and ACS-NT; Philips Medical Systems, Best, the Netherlands) by using a standard bilateral breast coil. The standardized protocol consisted of a T2-weighted turbo spin-echo sequence (field of view, 280–320 mm; 31 sections with 3-mm section thickness, without gap; 3,800/120 [repetition time msec/echo time msec]; turbo factor, 19; number of signals acquired, two; 512 x 406 matrix), followed by a dynamic series (two-dimensional gradient-echo technique) of five to seven dynamic image stacks (260/4.6; flip angle, 90°; full 256 x 256 or 512 x 400 matrix; 31 sections with a section thickness of 3 mm, without gap; field of view, 280–320 mm). The first series were obtained just before power injection of 0.1 mmol gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) per kilogram of body weight and a 20-mL flush of saline solution (3 mL/sec). The temporal resolution was 60–90 seconds for each dynamic acquisition, which yielded a total imaging time of 7 minutes. Image subtraction was performed to suppress the signal from fat.
Postprocessing of MR Imaging Data
Enhancement rates were quantified with region-of-interest–based analysis (17). Relative enhancement rates (percentage of signal intensity increase) were calculated according to the formula (SIc - SI)/SI x 100, where SI and SIc are signal intensities before and the first after, respectively, contrast enhancement. By plotting the signal intensity over time, signal intensity–time curves were generated for each enhancing lesion. A qualitative assessment of signal intensity–time courses was performed as described previously (17). An enhancement rate beyond 60% of the relative signal intensity increase within the first dynamic series was considered relevant.
Data Analysis
Findings of MR examinations were prospectively interpreted in consensus by two radiologists (N.M., C.K.K.) experienced in breast MR imaging. The radiologists were totally informed about clinical history and mammographic and US findings. Diagnoses were classified equivalent to the Breast Imaging Reporting and Data System (BI-RADS) categories. The following criteria were investigated (N.M., C.K.K., C.C.L.): visual (qualitative) assessment of structural changes, which took into consideration the presence or absence of cutaneous or parenchymal edema, and quantitative analysis of contrast enhancement by determining enhancement kinetics of the parenchyma.
For each breast, three regions of interest (mean size, 1 cm) were placed by one of the authors (N.M.) on the area with the strongest enhancement, as judged by the early postcontrast images; a mean value over the three regions of interest was calculated. Regions of interest identical in size and location were placed on the parenchyma of the nonirradiated breast to obtain intraindividual reference values.
For detection and classification of incidental contrast-enhancing lesions (lesions that do not correspond to a correlate on conventional images but are visible on breast MR images alone), we (N.M., C.K.K., C.C.L.) read the MR images according to the same interpretation guidelines that are in use for our patients at clinical breast MR examination (14,18,19).
We applied criteria related to lesion morphology, lesion internal architecture, and lesion contrast enhancement kinetics. If a lesion with relevant enhancement is identified, the first step is to assess whether it is a mass- or a non–mass-related enhancement. In case of non–mass-related segmental or ductal enhancement (corresponding to BI-RADS category 4 or 5), biopsy is recommended. If a focal mass is identified, lesion morphology is evaluated. In case smooth borders and internal septa are present, the lesion is classified as benign (BI-RADS category 2), irrespective of enhancement kinetics.
If the lesion appears irregular (BI-RADS category 4 equivalent), biopsy is recommended. If the lesion has smooth borders, evaluation of contrast enhancement dynamics is performed. If a wash-out time course is identified (BI-RADS category 4), biopsy is recommended. If a continuous enhancement or a plateau is identified (BI-RADS category 3), follow-up is performed. If both morphologic and kinetic criteria suggest malignancy, the lesion is classified as probably malignant (BI-RADS category 5).
Several further criteria such as lesion signal intensity on T2-weighted turbo spin-echo images, symmetry or asymmetry compared with that of the contralateral side, and progression of enhancement within a lesion, to name a few, are evaluated in conjunction with the just-mentioned criteria (14,19).
Statistical Analysis
For statistical analysis, a software package (Excel 2000; Microsoft, Redmond, Wash) was used. The mean values, ranges, and SDs of the enhancement rates in the irradiated and the contralateral breast were calculated; a two-tailed paired Student t test was performed to evaluate statistical significance. P < .01 was considered to indicate a significant difference.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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In group C, parenchymal enhancement rates of the irradiated breast were equivalent to those measured in the contralateral breast (irradiated breast: mean value, 24% ± 12; nonirradiated breast parenchyma: mean value, 21% ± 12). In none of the patients did the parenchymal enhancement rates reach diagnostically relevant levels (P = .09).
In group D, the mean enhancement rates of the irradiated breasts were again comparable throughout to those obtained in the contralateral breasts (P = .70).
Imaging Features of Focal Lesions
A total of 21 enhancing lesions were detected in irradiated breasts, and another 10 were identified in nonirradiated breasts (Table 1); the difference in the prevalence of enhancing lesions proved statistically significant (P < .01). The morphologic features and contrast enhancement characteristics of the malignant lesions identified in our study cohort are given in Table 2.
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Diagnostic Accuracy
On the basis of MR-guided biopsy or long-term follow-up findings, we had five true-positive, three false-positive, no false-negative, and 108 true-negative diagnoses in the irradiated breasts of the 116 MR studies in the 72 patients (Table 3). In the nonirradiated breasts, we had two true-positive, one false-positive, no false-negative, and 113 true-negative diagnoses. Table 4 provides the Bayesian variables for the irradiated and the nonirradiated breast. Sensitivity, specificity, negative predictive value, positive predictive value, and overall diagnostic accuracy were equivalent in the irradiated and the nonirradiated breast. No statistically significant difference was identified.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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High-frequency breast US may be problematic after breast-conserving therapy as well, because diffuse acoustic shadowing owing to scarring can mimic or obscure tumor recurrence (9).
Use of breast MR imaging is well accepted to improve differentiation of scar versus tumor recurrence when it is performed later than 12–18 months after the end of radiation therapy (10,13,25–30), whereas its use is broadly discouraged before this time point. This recommendation was based on the experience that radiation-induced inflammatory changes allegedly led to a diffuse and severe enhancement of the entire breast parenchyma, thus precluding identification of residual or recurrent breast cancer.
Our study was designed to specifically address the question of whether radiation-induced changes of contrast enhancement are such that they in fact impair identification and classification of enhancing lesions on dynamic contrast-enhanced MR images.
The issue concerning early postradiation breast MR imaging is in fact twofold: The first concern is that radiation-induced diffuse parenchymal enhancement may obscure or mimic residual or recurrent breast cancer. Second, it is possible that radiation therapy may modify (in particular, suppress) lesion enhancement rates such that irradiated residual breast cancer would not enhance any more and would therefore escape diagnosis. Both effects, increased enhancement of irradiated parenchyma and decreased enhancement of residual or recurrent breast cancer, are conceivable and both would severely impair the mere detection and correct classification of lesions in contrast-enhanced breast MR imaging studies.
Our data confirm data of previous studies (12,13) that radiation-induced inflammatory changes go along with parenchymal and skin edema and increased parenchymal enhancement. In group A, the mean parenchymal enhancement was 39% ± 26 on the irradiated side compared with 18% ± 15 on the nonirradiated side. However, an enhancement rate of 39% is well below relevant levels; it is hardly perceivable on subtracted MR images. Therefore, in our patients, the effect of radiation therapy on parenchymal enhancement was much less severe than was reported previously (12,13). Also, these rather subtle radiation therapy–induced effects subsided considerably faster than expected: Parenchymal enhancement rates peaked during radiation therapy, but already after 3 months, the difference was leveled out, and enhancement rates of the irradiated and the nonirradiated side were equivalent.
Disregarding mean values and considering the individual MR studies, we found that in group A (during radiation therapy), enhancement rates reached relevant levels in eight of 44 patients. However, in two of these patients, comparable enhancement rates were measured also in the respective contralateral breasts; this shows that relevant enhancement occurs spontaneously and is not necessarily attributable to previous radiation. In group B (up to 3 months after radiation therapy), relevant parenchymal enhancement was observed as often in the irradiated breasts as in the nonirradiated breasts; it was observed in one patient on the irradiated side and in one patient on the contralateral side only. In groups C and D, no further cases with relevant enhancement were observed in the irradiated breast. Therefore, the overall relevant parenchymal enhancement was demonstrated in nine (8%) of 116 studies on the irradiated side in three (3%) of 116 studies on the contralateral side (difference not statistically significant). On the basis of our prospective diagnoses, the (mildly) increased parenchymal enhancement in group A patients did not translate into a statistically significant reduction of diagnostic accuracy. Findings of short-term follow-up MR studies in all patients with relevant parenchymal enhancement showed that the enhancement rates returned to normal by 3–6 months. None of these patients had false-positive findings or underwent biopsies, and none of the patients were diagnosed with breast cancer at follow-up imaging.
Concerning parenchymal enhancement, our data suggest that in the majority of patients, including the period immediately after radiation therapy, the slightly increased contrast enhancement attributable to radiation therapy is not likely to mimic or obscure breast cancer.
In regard to whether radiation therapy influences MR imaging features, specifically enhancement kinetics, of benign and malignant lesions, medical therapy (in particular, systemic chemotherapy) is known to suppress enhancement of residual breast cancer such that false-negative MR diagnoses are possible during or immediately after chemotherapy (31). Our data suggest that radiation therapy does not interfere with (in particular, does not suppress) contrast enhancement characteristics of residual or recurrent breast cancers or of benign lesions. The imaging features of the five breast cancers identified in irradiated breasts corresponded well to those found in nonirradiated breasts. Moreover, enhancement rates and morphologic features corresponded well to breast cancers found in our regular patients with nonirradiated breasts.
It is always difficult to entirely exclude false-negative diagnoses as long as no histologic proof of the negative cases is obtained. Currently, a 2-year follow-up with conventional and MR imaging is considered sufficient to validate a negative imaging diagnosis. In none of our patients did a local recurrence occur during this follow-up period. Two patients did develop local recurrence, one at 3 years and one at 4 years after radiation therapy; yet, in none of these cases did we find any signs of breast cancer (eg, a nonenhancing focal mass at the site of subsequently diagnosed cancer) at minute comparison of study MR images and subsequent MR images. Although we cannot offer histologic validation for all of our negative MR diagnoses, on the basis of follow-up data we believe that we can confidently state that the probability of false-negative diagnoses secondary to nonenhancing breast cancers is very low.
We did observe a higher prevalence of benign contrast-enhancing lesions in the irradiated breasts (16 [14%] of 116 compared with eight [7%] of 116 on the contralateral side, Table 1). We speculate that the diffuse hyperemia associated with radiation therapy may lead to the increased enhancement (and thus an increased detectability and/or prevalence) of benign lesions. It is possible that these lesions are misinterpreted as residual or recurrent tumor and, therefore, may reduce the diagnostic accuracy of breast MR imaging. Yet, we were able to correctly classify 13 of the 16 lesions in the irradiated breast (seven of eight lesions in the contralateral breast) as probably benign, owing to their typical benign-appearing morphologic and kinetic features. Therefore, we were able to maintain a positive predictive value that was comparable to that of the nonirradiated side.
When we took into consideration that we were dealing with "high-risk" patients who were known to be treated for invasive breast cancer, we believe that we caused relatively few false-positive biopsy calls: Among the 72 patients, three false-positive diagnoses were made in irradiated breasts and one in nonirradiated breasts. This difference in numbers is, in our view, attributable to the fact that the irradiated breasts were known to be the site of a previous breast cancer rather than radiation-induced changes per se. In the same patient, the threshold to recommend biopsy for any given lesion is lower in the diseased and treated breast than it is in the presumably healthy contralateral side. Moreover, the type of lesions that gave rise to false-positive biopsy calls in our study cohort, that is, lymph nodes and fibroadenomas, are known to exhibit features that overlap with malignant lesions regardless of previous radiation therapy (32,33). Typical posttherapeutic changes (focal mastitis, enhancing fresh fat necrosis) were encountered less often than expected (five of 72 patients) and could be prospectively classified as such in all but one patient.
In the majority of patients in our cohort, neither detection nor correct classification of contrast-enhancing lesions was impaired after radiation therapy. This finding is in contrast to previous reports about the use of breast MR imaging as many as 24 months after radiation therapy (12,13). A possible explanation for this discrepancy is that first, in this systematic analysis, the radiation therapy–induced effects were found to be much less severe than reported. Second, we used several different diagnostic criteria for characterizing enhancing lesions. Previous reports that dealt with breast MR imaging after radiation therapy stem from a period when differential diagnosis in dynamic MR imaging relied on enhancement thresholds alone. With the additional interpretation of morphology and internal architecture and a critical analysis of the signal intensity–time curves (17) and signal intensity on the T2-weighted turbo spin-echo images (18), we were able to correctly classify the majority (13 of 16) of benign contrast-enhancing lesions (34,35) in the irradiated breast.
The second objective of our study was to investigate the prevalence of residual or recurrent breast cancer in patients who underwent breast-conservation therapy without preoperative breast MR imaging. In our study of 72 patients, we were able to prospectively diagnose unsuspected conventionally occult breast cancer in seven (10%) patients: In five patients, additional breast cancer was diagnosed in the irradiated breast (7%), and another two (3%) patients had unsuspected contralateral cancer. It is important to realize that in none of our patients had a preoperative breast MR imaging been performed. In our department, breast MR imaging has become an integral part of the preoperative work-up of patients who are considered candidates for breast-conserving therapy (36). However, many patients who presented to the radiation therapy section of our Department of Radiology underwent breast-conserving surgery elsewhere, and, thus, were not enrolled in our preoperative staging protocol. Tumor recurrence within the first months (or even weeks) after surgery is unusual, provided negative margins are obtained as is required by current standards of care. Therefore, we believe that it is much more probable that the unexpected breast cancer foci that became apparent at MR imaging represent residual conventionally occult multicentric breast cancer foci rather than recurrent disease.
The role of breast MR imaging for local staging has been increasingly established by recent publications by Orel and co-workers (36) and Fischer and co-workers (37). Our findings agree with those reported by Fischer and co-workers (37), who performed preoperative breast MR imaging to screen for additional conventionally occult breast cancer foci. They found additional breast cancers in 14% of patients; in our cohort, 10% (seven of 72) of patients had breast cancers that had apparently escaped the preoperative diagnosis based on mammography and high-resolution breast US. Thus, our data underscore the importance of preoperative breast MR imaging for local staging before breast-conservation therapy is initiated (15,38).
In conclusion, the use of breast MR imaging in the early period after radiation therapy has been discouraged, specifically owing to the allegedly severe diffuse contrast enhancement induced by radiation therapy. Our results show that in fact there were radiation-induced changes that were visible on breast MR images, but they were much less severe and subsided much faster than was previously reported. Moreover, when refined diagnostic criteria were used to distinguish benign from malignant enhancing lesions (rather than simple enhancement thresholds), these radiation-induced effects did not impair the diagnostic confidence of the interpreting radiologist and, as our prospective study findings show, did not translate into a reduced diagnostic accuracy. It should be well understood that we do not advocate the routine use of breast MR imaging in the early postirradiation period. Rather, we would recommend to use breast MR imaging preoperatively to improve local staging in patients who are candidates for breast-conservation surgery. This recommendation is underscored by the high prevalence of residual breast cancer that was found in our study group. However, our data do suggest that if inconclusive clinical or conventional (mammographic or US) imaging findings are obtained after breast-conserving therapy, contrast-enhanced MR imaging can be used effectively as a problem-solving tool, even during or soon after radiation therapy.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, C.K.K.; study concepts, C.K.K., N.M.; study design, C.K.K., N.M., C.C.L.; literature research, A.S., C.C.L.; clinical studies, N.M., C.C.L., A.S., C.K.K.; data acquisition, N.M., C.K.K., A.S., C.C.L.; data analysis/interpretation, C.K.K., N.M., C.C.L., H.H.S.; statistical analysis, N.M., C.K.K.; manuscript preparation and editing, N.M., C.K.K.; manuscript definition of intellectual content and revision/review, N.M., C.K.K., H.H.S.; manuscript final version approval, C.K.K., N.M., C.C.L., H.H.S.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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re JM, Shapeero LG, et al. Assessment of breast cancer recurrence with contrast-enhanced subtraction MR imaging: preliminary results in 26 patients. Radiology 1993; 188:473.This article has been cited by other articles:
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  C. K. Kuhl Current Status of Breast MR Imaging * Part 2. Clinical Applications Radiology, September 1, 2007; 244(3): 672 - 691. [Abstract] [Full Text] [PDF]
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C. K. Kuhl, P. Jost, N. Morakkabati, O. Zivanovic, H. H. Schild, and J. Gieseke Contrast-enhanced MR Imaging of the Breast at 3.0 and 1.5 T in the Same Patients: Initial Experience Radiology, June 1, 2006; 239(3): 666 - 676. [Abstract] [Full Text] [PDF]
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N. Morakkabati-Spitz, H. H. Schild, C. C. Leutner, M. von Falkenhausen, G. Lutterbey, and C. K. Kuhl Dynamic Contrast-enhanced Breast MR Imaging in Men: Preliminary Results Radiology, December 21, 2005; (2005) 2382041312. [Abstract] [Full Text]
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C. K. Kuhl, H. H. Schild, and N. Morakkabati Dynamic Bilateral Contrast-enhanced MR Imaging of the Breast: Trade-off between Spatial and Temporal Resolution Radiology, September 1, 2005; 236(3): 789 - 800. [Abstract] [Full Text] [PDF]
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