Annals of Surgical Oncology Cite Track
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Hwang, E. S.
Right arrow Articles by Hylton, N. M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Hwang, E. S.
Right arrow Articles by Hylton, N. M.
Related Collections
Right arrow Diagnosis
Annals of Surgical Oncology 10:381-388 (2003)
© 2003 Society of Surgical Oncology

ORIGINAL ARTICLES

Magnetic Resonance Imaging in Patients Diagnosed With Ductal Carcinoma-In-Situ: Value in the Diagnosis of Residual Disease, Occult Invasion, and Multicentricity

E. Shelley Hwang, MD, Karen Kinkel, MD, Laura J. Esserman, MD, Ying Lu, PhD, Noel Weidner, MD and Nola M. Hylton, PhD

From the Departments of Surgery (ESH, LJE), Pathology (NW), and Radiology (KK, YL, NMH), University of California–San Francisco, San Francisco, California.

Correspondence: Address correspondence and reprint requests to: E. Shelley Hwang, MD, UCSF Department of Surgery, 1600 Divisadero Street, Room B611, San Francisco, CA 94115; Fax: 415-353-9571; E-mail: shelley.hwang{at}ucsfmedctr.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Although magnetic resonance imaging (MRI) has been shown to be a sensitive imaging tool for invasive breast cancers, its utility in ductal carcinoma-in-situ (DCIS) of the breast remains controversial. We studied the performance of MRI in patients with known DCIS for assessment of residual disease, occult invasion, and multicentricity to determine the clinical role of MRI in this setting.

Methods: Fifty-one patients with biopsy-proven DCIS underwent contrast-enhanced MRI before surgical treatment. Pre-, early post-, and late postcontrast three-dimensional gradient echo images were obtained and MRI findings were correlated with histopathology. When possible, the performance of MRI and mammography was compared.

Results: The accuracy of MRI was 88% in predicting residual disease, 82% in predicting invasive disease, and 90% in predicting multicentricity. The performance of MRI was equivalent in the core biopsy group when compared with the surgical biopsy group. For occult invasion only, MRI and mammography were equivalent. However, overall, MRI was more sensitive and had a higher negative predictive value than mammography.

Conclusions: MRI of DCIS can serve as a useful adjunct to mammography by providing a more accurate assessment of the extent of residual or multicentric disease. The performance of MRI is not significantly affected by antecedent surgical excision. MRI may be particularly valuable if preoperatively negative.

Key Words: Breast cancer • Ductal carcinoma-in-situ • Magnetic resonance imaging • Comparative studies • Mammography


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Ductal carcinoma-in-situ (DCIS) of the breast currently represents approximately 20% to 40% of all mammographically detected breast cancers, and it is estimated that >50,000 new cases are diagnosed yearly in the United States.1–3 The natural history of DCIS is still not well understood, but early studies that reported long-term follow-up of patients treated for DCIS with biopsy showed a recurrence rate of 10% to 63%, half of which were invasive cancers.4–7 This supports the current model for DCIS progression, which argues that in situ disease is a precursor of invasive cancer.8

The current surgical recommendation for DCIS is complete excision. Often, this entails a mastectomy, because the true extent of disease has been difficult to assess with the standard diagnostic modalities used currently. However, subgross sectioning of mastectomy specimens in patients with DCIS suggests that most women with this diagnosis have disease confined to a single quadrant.9 They are thus candidates for breast-conserving surgery, provided that the true extent of their disease can be assessed before surgical intervention.

Critical questions requiring answers for treatment planning are (1) Does the patient have residual disease necessitating further surgery? (2) Is there associated invasive cancer that would require axillary node assessment? and (3) Is there multicentric disease precluding breast-conserving surgery? Although mammography can detect up to 83% of DCIS lesions,10 it has been shown to consistently underestimate the extent of disease, especially in the setting of postoperative changes.11,12 In addition, the overlapping morphological features between invasive cancer and DCIS on mammography limit the utility of this modality in the detection of occult invasive disease.13

Recent studies have demonstrated that for invasive cancers, magnetic resonance imaging (MRI) is more accurate than mammography in assessing both tumor size and multifocality.14,15 Although numerous small studies describe morphologic or kinetic enhancement characteristics of DCIS,16–18 little is known regarding the accuracy of MRI compared with mammography in the evaluation of DCIS or regarding the potential role of MRI in treatment planning. We therefore undertook a prospective study to determine whether MRI of the breast could refine preoperative decision-making in those patients diagnosed with DCIS alone.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From 1996 to 1999, 190 patients with known breast cancer underwent MRI of the breast before undergoing surgical treatment at our institution. Among those, 51 patients (27%) had a histologically confirmed diagnosis of DCIS alone at the time of MRI examination, and these patients constitute our study population. The study was approved by the institutional review board, and informed consent was obtained from all patients before study participation.

MRI Acquisition and Interpretation
MRI was performed on a Signa system (GE Medical Systems, Milwaukee, WI) at 1.5 T. All patients were imaged in a prone position in a dedicated double breast coil. The breast with the known diagnosis of DCIS was imaged. A transverse T1-weighted spin echo sequence was performed for localization purposes and was followed by a sagittal, fat-suppressed T2-weighted fast spin echo sequence for the identification of cystic structures. A three-dimensional, sagittal, fat-suppressed T1-weighted fast gradient recalled echo sequence was obtained before, at 2 minutes 30 seconds, and at 7 minutes 30 seconds after a bolus injection of .1 mmol/kg of gadolinium diethylenetriamine pentaacetic acid (Magnevist; Berlex Laboratories Inc., Wayne, NJ). The following parameters were used: repetition time, 11.0 msec; echo time, 4.2 msec; field of view, 18 cm; matrix, 256 x 192; slice thickness, 2.0 mm with no gap; two signals averaged; and spectrally selected, inversion recovery-prepared fat suppression. Reformatted images in a craniocaudal, mediolateral, or anterior-posterior projection (maximum-intensity projection) were created from precontrast, early postcontrast, and late postcontrast three-dimensional, sagittal, fat-suppressed T1-weighted fast gradient recalled echo sequence data sets, each containing 60 sections.

The images were prospectively analyzed for both morphological and dynamic imaging parameters. The morphological lesion type (i.e., mass vs. nonmass) was classified by following guidelines for magnetic resonance lesion description according to a technical report of the Public Health Service Office of Women’s Health.18 Regional or segmental non–mass-like enhancements were described as stippled, clumped, heterogeneous, or homogeneous. The margins of ductal enhancement were classified as regular or irregular. Kinetic contrast-enhancement characteristics, including the degree of enhancement and the enhancement pattern over time (i.e., washout, plateau, or progressive enhancement), were noted for each lesion type. All imaging data were collected prospectively before surgical intervention. MRIs were analyzed by radiologist A, who was blinded to both pathology and mammography.

Diagnostic criteria for invasive disease consisted of (1) the presence of a spiculated mass or (2) the presence of an enhancing mass with subsequent washout and nonsmooth margins (Fig. 1). Diagnostic criteria for DCIS were (1) nonstippled regional or segmental enhancement or (2) irregular ductal enhancement (Fig. 2). All other focal mass or nonmass enhancements were considered benign. Multicentricity was diagnosed if the volume of suggestive enhancement extended over at least 25% of the breast volume, corresponding to an area larger than one quadrant (Fig. 3A and B), or if multiple foci of disease occupied more than one quadrant.



View larger version (171K):
[in this window]
[in a new window]
  		FIG. 1. A 48-year-old patient diagnosed with ductal carcinoma-in-situ (DCIS) after a core biopsy. The postoperative postcontrast magnetic resonance image shows a focal mass with slightly spiculated borders corresponding to invasive cancer and an anterior portion of irregular linear enhancement corresponding to a focus of DCIS at histopathology.

 


View larger version (157K):
[in this window]
[in a new window]
  		FIG. 2. A 44-year-old patient diagnosed with ductal carcinoma-in-situ (DCIS) and positive margins after a surgical biopsy in the upper outer quadrant. The postoperative magnetic resonance image shows multifocal irregular linear ductal enhancement. Histopathology of the mastectomy specimen showed multifocal DCIS in the lower outer quadrant.

 


View larger version (76K):
[in this window]
[in a new window]
  		FIG. 3. A 39-year-old patient diagnosed with ductal carcinoma-in-situ (DCIS) after a core biopsy for microcalcifications. Maximum-intensity projections of contrast-enhanced three-dimensional high-spatial-resolution magnetic resonance imaging in a craniocaudal (A) and sagittal (B) projection demonstrate suggestive clumped and homogeneous regional enhancement in both the upper outer and lower outer quadrants. Histopathology of the mastectomy specimen confirmed the presence of multicentric DCIS in the outer quadrants.

 
Mammography
All patients underwent mammography at the time of initial diagnosis, and 33 (65%) had microcalcifications as the first presentation of DCIS. In 38 of 51 patients, a mammogram was obtained after biopsy (either core biopsy or surgical excision), before surgical treatment, and within 6 weeks of MRI. The mammogram consisted of mediolateral and craniocaudal views without spot magnification in seven patients. In 28 patients, additional spot magnification views were also obtained. In three patients, spot magnification views were the only available mammographic images; the insufficient assessment of the remainder of the breast did not allow for mammographic assessment of multicentricity in these patients. Mammography was assessed by radiologist B, who was blinded to pathology and the results of MRI.

Histopathologic Correlation
Histopathologic correlation between MRI and histology slides was performed according to routine tissue-processing procedures at our institution. During surgery, all specimens were precisely oriented to provide strict anatomical correlation to the in vivo tumor. All specimens were serially sectioned sagittally from medial to lateral margins. The size of DCIS was recorded as the single greatest measurement in one dimension. Grade was scored as low, intermediate, or high. The surgical specimen was also carefully assessed for any associated, previously occult invasive cancer. The extent of disease within the specimen was classified as unicentric or multicentric, with multicentricity defined as tumor within at least two quadrants.

Data Analysis
The sensitivity, specificity, accuracy, and positive and negative predictive values were calculated for both mammography and MRI in the evaluation of residual DCIS, occult invasive disease, and multicentricity. Because some subjects in the study did not have correlating mammography within 6 weeks of the MRI, the denominators used to calculate the rates of residual, invasive, and multicentric disease were different for mammography and MRI. Thus, the McNemar test was not applicable. Instead, we used the bootstrap approach19 to compare the differences in efficacy for mammography and MRI.19,20 If a 95% bootstrap confidence interval did not contain 0, the difference was considered significantly different at the .05 level.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient and Tumor Characteristics
The study population consisted of 51 patients with histologically confirmed DCIS alone. The modes of presentation at the time of diagnosis, including suggestive mammogram, palpable mass, or nipple discharge, as well as tumor grade, are listed in Table 1.


View this table:
[in this window]
[in a new window]
  		TABLE 1. Clinical and pathologic characteristics of 51 patients diagnosed with ductal carcinoma-in-situ only on core or surgical biopsy
 
Before MRI, the diagnosis of DCIS was obtained by core biopsy in 17 (33%) of 51 cases (Figs. 1 and 3) and by open surgical biopsy in the remaining 34 patients (67%; Figs. 2 and 4). Of the 34 patients who had undergone surgical biopsy, 7 had also had a re-excision for close or positive margins before the MRI. In 39 patients, nuclear grade was obtained from a prior core or surgical biopsy, of which the highest grade was recorded. Twenty-three patients had associated comedo necrosis. All patients included in the study underwent surgical treatment within 6 weeks of the MRI examination; this consisted of wide excision in 25 patients and mastectomy in 26 patients. Histological assessment of these specimens revealed residual DCIS in 39 patients. Occult invasive cancer was seen in 7 patients and multicentricity in 16 patients.



View larger version (181K):
[in this window]
[in a new window]
  		FIG. 4. A 45-year-old patient diagnosed with ductal carcinoma-in-situ (DCIS) after a surgical biopsy of a palpable mass. The postoperative postcontrast magnetic resonance image shows an irregular branching ductal enhancement corresponding to residual multifocal DCIS at histopathology.

 
Performance of MRI
The sensitivity and specificity of MRI for predicting residual disease, associated invasive cancer, and multicentric DCIS were calculated for the overall group, as well as for two subgroups, depending on the type of prior biopsy (core vs. surgical biopsy) undertaken most antecedent to the MRI examination (Table 2). In the overall group, the sensitivity of MRI was greatest for the detection of residual DCIS (97%), and the specificity was best in the evaluation of multicentricity (89%). The sensitivity and specificity of MRI in the detection of residual disease, invasive cancer, and multicentricity was not significantly superior in the core biopsy–only group when compared with the group in which the diagnosis of DCIS was obtained by surgical biopsy.


View this table:
[in this window]
[in a new window]
  		TABLE 2. Sensitivity and specificity of magnetic resonance imaging in predicting residual disease, occult invasion, and multicentricity in patients diagnosed with ductal carcinoma-in-situ on core biopsy or surgical biopsy
 
Comparison of MRI to Mammography
In the 38 patients for whom correlating mammograms were obtained after histological diagnosis and within 6 weeks of the MRI examination, the performance of mammography in the detection of residual disease, associated invasive cancer, and multicentric DCIS was calculated and compared with that of MRI (Table 3). The differences in sensitivity, specificity, accuracy, positive predictive value, and negative predictive value between mammography and MRI are listed in Table 4, and the statistical significance of each difference is presented. A negative difference suggested a better performance for MRI. With the bootstrap method and a significance level of 5%, MRI had significantly higher sensitivities and negative predictive values than mammography in the detection of residual disease, occult invasive cancer, and multicentric DCIS. MRI also had statistically significantly higher accuracy in detection of multicentric DCIS. However, MRI had significantly lower specificity than mammography for detection of associated invasive cancer.


View this table:
[in this window]
[in a new window]
  		TABLE 3. Comparison of performance of mammography and MRI in predicting residual disease, occult invasion, and multicentricity in patients diagnosed with ductal carcinoma-in-situ only at biopsy
 

View this table:
[in this window]
[in a new window]
  		TABLE 4. Bootstrap statistical analysis of observed differences between mammography (MMG) and magnetic resonance imaging (MRI)
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Despite recent advances in the diagnosis, evaluation, and treatment of breast cancers, the surgical treatment of DCIS remains imprecise. One of the greatest barriers to accurate surgical resection remains the difficulty in preoperative assessment of this disease. Not uncommonly, a small area of microcalcifications on mammography is the only detectable abnormality, although the true extent of disease may span the entire breast or may be present in multiple foci. Thus, additional radiographical assessment by a more sensitive modality, such as MRI, has the potential to refine clinical decision-making for DCIS.

Previous studies have demonstrated the potential of MRI in this regard. Although early experience suggested that the sensitivity of MRI for DCIS was low compared with that for invasive cancer,21,22 subsequent small studies have shown improvements in both the sensitivity and specificity of MRI for intraductal cancers. In one study of purely DCIS lesions, eight of nine cases were visualized on MRI.23 Furthermore, the authors showed that in this small group, MRI was better at predicting multifocality than either mammography or ultrasound. Another retrospective report of 22 patients with DCIS alone or DCIS with associated invasive cancer found abnormal enhancing characteristics in every case.24 It is interesting to note that five of these patients had had surgical biopsies before undergoing MRI, but this did not reduce accuracy for diagnosing tumor extent in this group. In the largest reported retrospective experience of MRI in DCIS to date, 34 of 36 cases of DCIS had an MRI correlate.16

Improvements in the MRI techniques used for breast imaging may at least partially explain this improved performance. Investigators using high-temporal-resolution MRI showed a lower sensitivity for DCIS than for invasive cancer.21 In contrast, studies using a high-spatial-resolution technique demonstrated greater sensitivity and specificity of MRI in the assessment of DCIS.24 Our technique combined both intermediate spatial and temporal resolution, allowing the assessment of both morphological and dynamic lesion enhancement characteristics. With this technique, the sensitivity of MRI for detecting residual disease, occult invasion, or multicentricity was high. It is interesting to note that subset analysis did not reveal a statistically significant difference in sensitivity and specificity for MRI in those patients who had undergone surgical biopsy versus core biopsy alone. Thus, even those patients with DCIS who have undergone prior surgery may still benefit from MRI. Clinical examination, mammography, and ultrasound have been shown to be poor predictors of the presence or extent of residual disease.25,26 Our data show that in the group that has undergone prior surgery, the sensitivity of MRI for detection of residual disease and multicentricity remains impressive (96% and 86%, respectively). Others have shown similar results for prediction of residual breast cancer after surgical excision in a study that included invasive and in situ tumors.27 It is important to note, however, that recent studies have pointed to the importance of delaying MRI examinations after surgical procedures. Indeed, if MRI is performed earlier than 1 month after surgery, the specificity in the diagnosis of residual cancer decreases from 73% to 42%.28

All 51 patients underwent mammography as part of their initial work-up. However, only 38 of 51 patients had a mammogram within 6 weeks of the MRI and before surgery, as the need for repeat mammography was left to individual physician discretion. Any mammograms performed greater than 6 weeks before the MRI were excluded from analysis because of possible introduction of bias favoring MRI examinations. In those patients for whom correlating mammograms were obtained, comparison of MRI with mammography demonstrates that the sensitivity and negative predictive value of MRI are superior to those of mammography for the detection of residual DCIS, occult invasive cancer, and multicentricity. Thus, residual disease, occult invasive cancer, and multicentric disease can be confidently ruled out with a negative MRI. In those cases of prior surgery with positive margins and a negative preoperative MRI, a small re-excision to establish negative margins may be all that is required for definitive surgical treatment. Because the positive predictive value was not significantly different between MRI and mammography, a suggestive finding on MRI was no more indicative of residual DCIS, invasive cancer, or multicentric disease than a suggestive mammogram. Nevertheless, the greater sensitivity seen with MRI suggests that if DCIS or invasive cancer is present, it is more likely to be demonstrated with MRI than mammography.

Both mammography and MRI demonstrated a low positive predictive value for the assessment of occult invasion (50% and 43%, respectively). In the overall group, six of seven patients had concomitant invasive cancer detected by MRI. However, eight patients with no invasive cancer had findings on MRI that were suggestive of invasion. Undoubtedly, this result can at least partially be attributed to the high degree of sensitivity of this imaging modality. Among patients who had a correlating mammogram, the presence or absence of invasive cancer was accurately predicted mammographically in only 30 of 38 patients. Thus, if occult invasive cancer is suspected, only a negative MRI can help determine whether a concomitant sentinel lymph node biopsy is indicated. If a preoperative MRI or mammogram is indeterminate, the likelihood of occult invasion must be predicted on the basis of clinical parameters such as tumor grade and size or the presence of comedo necrosis, with surgery to the axilla planned accordingly.

We acknowledge that our study cohort was not entirely representative of the larger population of patients with DCIS. A significant number of women in our study had undergone primary treatment elsewhere and were referred specifically for assessment of residual disease. These patients may have been somewhat self-selected, with a higher percentage requiring re-excision or mastectomy. Nevertheless, we believe that this did not affect our assessment of the performance of MRI and, rather, allowed us to identify those clinical situations in which MRI could have the greatest utility.

We are continuing to explore the many potential uses of this technology in the evaluation of breast disease. In high-risk populations, such as those with known BRCA mutations, MRI screening may have a role. Another group that may benefit is those patients with very dense or nodular breasts, in whom mammography or clinical examination may be less reliable. The improving ability to perform for MRI-guided interventions will increase the utility of this technology. However, MRI is an expensive diagnostic modality, and in an era of cost-containment in health care, it is imperative that new technology be used judiciously. Ongoing cost-benefit analyses will help determine whether breast MRI can be justified by its potential effects on earlier detection or improved treatment planning.

We conclude that in those patients with DCIS clinically suspected to have residual disease, occult invasive cancer, or multicentric disease, a negative MRI may help limit the need for extensive surgical intervention, even in the setting of prior surgical excision. In cases of a large tumor-breast ratio, MRI may allow for more precise surgical planning. This could reduce the need for mastectomy or multiple repeat excisions.


   Acknowledgments
 
The authors thank Nina Jaaj for her assistance in preparation of this manuscript. Supported by a grant (97-036-01-EDT) from the American Cancer Society.

The acknowledgments are available online at www.annalssurgicaloncology.org.


   Footnotes
 
The value of breast magnetic resonance imaging (MRI) in the management of ductal carcinoma-in-situ (DCIS) was evaluated in a prospective study of patients diagnosed with DCIS only. When compared with mammography, MRI was more sensitive for the diagnosis of residual disease, occult invasive cancer, and multicentricity. MRI performance was not affected by prior surgical excision.

Received for publication March 28, 2002. Accepted for publication November 7, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Ernster VL, Barclay J. Increases in ductal carcinoma in situ (DCIS) of the breast in relation to mammography: a dilemma. J Natl Cancer Inst Monogr 1997; 22: 151–6.
  2. Greenlee RT, Murray T, Bolden S, Wingo PA. Cancer statistics, 2000. CA Cancer J Clin 2000; 50: 7–33.[Abstract]
  3. Recht A, Rutgers EJ, Fentiman IS, Kurtz JM, Mansel RE, Sloane JP. The fourth EORTC DCIS Consensus meeting (Chateau Marquette, Heemskerk, The Netherlands, 23–24 January 1998)—conference report. Eur J Cancer 1998; 34: 1664–9.
  4. Gallagher WJ, Koerner FC, Wood WC. Treatment of intraductal carcinoma with limited surgery: long-term follow-up. J Clin Oncol 1989; 7: 376–80.[Abstract]
  5. Lagios MD, Margolin FR, Westdahl PR, Rose MR. Mammographically detected duct carcinoma in situ. Frequency of local recurrence following tylectomy and prognostic effect of nuclear grade on local recurrence. Cancer 1989; 63: 618–24.[CrossRef][Medline]
  6. Graham RA, Homer MJ, Sigler CJ, et al. The efficacy of specimen radiography in evaluating the surgical margins of impalpable breast carcinoma. AJR Am J Roentgenol 1994; 162: 33–6.[Abstract/Free Full Text]
  7. Schwartz GF, Finkel GC, Garcia JC, Patchefsky AS. Subclinical ductal carcinoma in situ of the breast. Treatment by local excision and surveillance alone. Cancer 1992; 70: 2468–74.[CrossRef][Medline]
  8. Beckmann MW, Niederacher D, Schnurch HG, Gusterson BA, Bender HG. Multistep carcinogenesis of breast cancer and tumour heterogeneity. J Mol Med 1997; 75: 429–39.[CrossRef][Medline]
  9. Faverly DR, Burgers L, Bult P, Holland R. Three dimensional imaging of mammary ductal carcinoma in situ: clinical implications. Semin Diagn Pathol 1994; 11: 193–8.[Medline]
  10. Fisher B, Costantino J, Redmond C, et al. Lumpectomy compared with lumpectomy and radiation therapy for the treatment of intraductal breast cancer. N Engl J Med 1993; 328: 1581–6.[Abstract/Free Full Text]
  11. Holland R, Hendriks JH, Vebeek AL, Mravunac M, Schuurmans Stekhoven JH. Extent, distribution, and mammographic/histological correlations of breast ductal carcinoma in situ. Lancet 1990; 335: 519–22.[CrossRef][Medline]
  12. Stomper PC, Connolly JL. Ductal carcinoma in situ of the breast: correlation between mammographic calcification and tumor subtype. AJR Am J Roentgenol 1992; 159: 483–5.[Abstract/Free Full Text]
  13. Sickles EA. Mammographic features of 300 consecutive nonpalpable breast cancers. AJR Am J Roentgenol 1986; 146: 661–3.[Abstract/Free Full Text]
  14. Mumtaz H, Hall-Craggs MA, Davidson T, et al. Staging of symptomatic primary breast cancer with MR imaging. AJR Am J Roentgenol 1997; 169: 417–24.[Abstract/Free Full Text]
  15. Esserman LJ, Hylton NM, Yassa NM, et al. Utility of magnetic resonance imaging in the management of breast cancer: evidence for improved preoperative staging. J Clin Oncol 1999; 17: 110–9.[Abstract/Free Full Text]
  16. Gilles R, Zafrani B, Guinebretiere JM, et al. Ductal carcinoma in situ: MR imaging-histopathologic correlation. Radiology 1995; 196: 415–9.[Abstract/Free Full Text]
  17. Orel SG, Mendonca MH, Reynolds C, Schnall MD, Solin LJ, Sullivan DC. MR imaging of ductal carcinoma in situ. Radiology 1997; 202: 413–20.[Abstract/Free Full Text]
  18. Harms SE. Technical report of the international working group on breast MRI. J Magn Reson Imaging 1999; 10: 979.[CrossRef][Medline]
  19. Efron B, Tibshirani RJ. An Introduction to the Bootstrap. London: Chapman & Hall, 1993.
  20. Bentzen SM. Prognostic factor studies in oncology: osteosarcoma as a clinical example. Int J Radiat Oncol Biol Phys 2001; 49: 513–8.[CrossRef][Medline]
  21. Orel SG, Schnall MD, LiVolsi VA, Troupin RH. Suspicious breast lesions: MR imaging with radiologic-pathologic correlation. Radiology 1994; 190: 485–93.[Abstract/Free Full Text]
  22. Boetes C, Strijk SP, Holland R, Barentsz JO, Van Der Sluis RF, Ruijs JH. False-negative MR imaging of malignant breast tumors. Eur Radiol 1997; 7: 1231–4.[CrossRef][Medline]
  23. Boetes C, Mus RD, Holland R, et al. Breast tumors: comparative accuracy of MR imaging relative to mammography and US for demonstrating extent. Radiology 1995; 197: 743–7.[Abstract/Free Full Text]
  24. Soderstrom CE, Harms SE, Copit DS, et al. Three-dimensional RODEO breast MR imaging of lesions containing ductal carcinoma in situ. Radiology 1996; 201: 427–32.[Abstract/Free Full Text]
  25. Peters ME, Fagerholm MI, Scanlan KA, Voegeli DR, Kelcz F. Mammographic evaluation of the postsurgical and irradiated breast. Radiographics 1988; 8: 873–99.[Abstract]
  26. Hassell PR, Olivotto IA, Mueller HA, Kingston GW, Basco VE. Early breast cancer: detection of recurrence after conservative surgery and radiation therapy. Radiology 1990; 176: 731–5.[Abstract/Free Full Text]
  27. Soderstrom CE, Harms SE, Farrell RS Jr, Pruneda JM, Flamig DP. Detection with MR imaging of residual tumor in the breast soon after surgery. AJR Am J Roentgenol 1997; 168: 485–8.[Abstract/Free Full Text]
  28. Frei KA, Kinkel K, Bonel HM, Lu Y, Esserman LJ, Hylton NM. MR imaging of the breast in patients with positive margins after lumpectomy: influence of the time interval between lumpectomy and MR imaging. AJR Am J Roentgenol 2000; 175: 1577–84.[Abstract/Free Full Text]



This article has been cited by other articles:


Home page
 RadiologyHome page
N. H. G. M. Peters, I. H. M. Borel Rinkes, N. P. A. Zuithoff, W. P. T. M. Mali, K. G. M. Moons, and P. H. M. Peeters
Meta-Analysis of MR Imaging in the Diagnosis of Breast Lesions
Radiology, December 1, 2007; 246(1): 116 - 124.
[Abstract] [Full Text] [PDF]

Home page
 RadiologyHome page
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]

Home page
 RadiologyHome page
C. Kuhl
The Current Status of Breast MR Imaging * Part I. Choice of Technique, Image Interpretation, Diagnostic Accuracy, and Transfer to Clinical Practice
Radiology, August 1, 2007; 244(2): 356 - 378.
[Abstract] [Full Text] [PDF]

Home page
 JCOHome page
L. J. Esserman, A. S. Kumar, A. F. Herrera, J. Leung, A. Au, Y.-Y. Chen, D. H. Moore, D. F. Chen, J. Hellawell, D. Wolverton, et al.
Magnetic Resonance Imaging Captures the Biology of Ductal Carcinoma In Situ
J. Clin. Oncol., October 1, 2006; 24(28): 4603 - 4610.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Roentgenol.Home page
C. D. Lehman, S. Peacock, W. B. DeMartini, and X. Chen
A new automated software system to evaluate breast MR examinations: improved specificity without decreased sensitivity.
Am. J. Roentgenol., July 1, 2006; 187(1): 51 - 56.
[Abstract] [Full Text] [PDF]

Home page
 J Am Board Fam MedHome page
S. K. Shah, S. K. Shah, and K. V. Greatrex
Current Role of Magnetic Resonance Imaging in Breast Imaging: A Primer for the Primary Care Physician
J Am Board Fam Med, November 1, 2005; 18(6): 478 - 490.
[Abstract] [Full Text] [PDF]

Home page
 RadiologyHome page
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]

Home page
 JCOHome page
N. Hylton
Magnetic Resonance Imaging of the Breast: Opportunities to Improve Breast Cancer Management
J. Clin. Oncol., March 10, 2005; 23(8): 1678 - 1684.
[Full Text] [PDF]

Home page
 JNCI J Natl Cancer InstHome page
G. D. Leonard and S. M. Swain
Ductal Carcinoma In Situ, Complexities and Challenges
J Natl Cancer Inst, June 16, 2004; 96(12): 906 - 920.
[Abstract] [Full Text] [PDF]

Home page
 Arch SurgHome page
F. H. Bagley
The Role of Magnetic Resonance Imaging Mammography in the Surgical Management of the Index Breast Cancer
Arch Surg, April 1, 2004; 139(4): 380 - 383.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Hwang, E. S.
Right arrow Articles by Hylton, N. M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Hwang, E. S.
Right arrow Articles by Hylton, N. M.
Related Collections
Right arrow Diagnosis

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS