Review of breast MRI: Indications and limitations

R e v i e w o f B r e a s t M R I : I n d i c a t i o n s and L i m i t a t i o n s Elizabeth A. Morris

HE MAMMOGRAM remains the only test that has been proven to reduce mortality of breast cancer. Nevertheless, mammography is limited in breasts that are difficult to image, such as dense breasts, augmented breasts, and breasts that have undergone breast conservation and radiation. The false-negative rate of mammography ranging from 5% to 15% 1 has prompted investigation into other modalities for breast cancer detection. Of all the techniques that have been investigated, magnetic resonance imaging (MRI) has the highest sensitivity and can provide valuable information that is not appreciated on the mammogram. Breast MRI performed for cancer detection requires the use of an intravenous contrast agent, such as gadolinium-diethylenetriamine pentaacetic acid (Gd-DTPA), which is taken up by areas of the breast where there is increased vascularity. Malignant lesions exhibit an increased number of blood vessels and increased vascular permeability due to leaky endothelial ceils. When contrast is injected, malignant lesions will generally enhance rapidly and strongly. Malignant lesions also demonstrate washout that is defined as a decrease in enhancement after peak enhancement has been reached. Washout is thought to result from increased vascular permeability and the presence of arteriovenous shunts. 2 In general, breast cancers enhance more rapidly and washout faster than benign lesions. However, there is overlap of enhancement features between malignant and benign lesions. For example, infiltrating lobular carcinoma, medullary carcinoma, and ductal carcinoma in situ (DCIS) can demonstrate slow uptake of contrast and no washout, mimicking a benign lesion. Or, these lesions may not take up contrast at all, producing a false-negative examination. 3 Conversely, false-positive examinations can be seen in virtually all types of benign pathology in the breast, such as fibroadenomas, recent scars,

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From the Department of Radiology, Weill Medical College of Cornell University, and Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021. Address reprint requests to Elizabeth A. Morris, MD, Department of Radiology, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021. Copyright 9 2001 by W.B. Saunders Company 0037-198X/01/3603-0008535.00/0 doi:10.1053/sroe.2001.25123 226

inflammatory processes, proliferative and nonproliferative changes, atypia, sclerosing adenosis, radial scar, and lobular carcinoma in situ (Fig 1). Any breast pathology with increased vascularity will demonstrate enhancement. Therefore, when interpreting breast MRI examinations, one cannot rely on enhancement alone. A combination of kinetic and morphologic features of the enhancement help decide which lesions warrant biopsy and which lesions can be watched. Clinical indications for breast MRI include preoperative staging where MRI has been shown to be extremely robust, detecting occult multifocal and multicentric disease that evaded detection clinically or with conventional imaging methods. 4-7 In the evaluation of recurrence (Fig 2) in the conserved breast where there is a question of scar versus recurrence, MRI has been shown to be superior to conventional imaging and physical examination. 8 In the assessment of residual disease following recent lumpectomy with positive or close margins (Fig 3), MRI can be performed in the early postoperative period to quantify the amount of residual disease remaining in the breast. 9 In the assessment of treatment response for locally advanced breast cancer (Fig 4), MRI can depict response to the prescribed chemotherapy regimen after a few cycles, which allows therapeutic decisions to be made more quickly and accurately than with clinical examination or mammography. Lo MRI is the gold standard in the assessment of mammographically occult carcinoma (Fig 5), particularly for those patients presenting with metastatic disease to the axilla and a negative mammogram and physical examination. 11,12 Additionally, MRI can be invaluable in the evaluation of the problematic mammogram and ultrasonography. 13 Finally, there is preliminary information that MRI may play a role in high-risk screening (Fig 6), although these data are early and final recommendations regarding use of MRI in this clinical setting are evolving.~4 LIMITATIONS

False-positive findings can pose a significant problem in the interpretation of breast MRI. The rate of false-positives varies greatly in the literature as the reported specificity ranges from 37% to 100~ 4,15-17 The large range of specificity can be

Seminars in Roentgenology, Vol XXXVI, No 3 (July), 2001: pp 226-237

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B Fig 1. False-positive MRI. A 54-year-old woman at high risk for breast cancer who had previously undergone multiple benign biopsies in both breasts underwent screening breast MRI examination. (A) Post-gadolinium-DTPA fat-suppressed sagittal Tl-weighted 3D gradient-echo image demonstrates a heterogeneously enhancing round smooth mass (open arrow) and two other foci of enhancement (solid arrows), (B) An MR-guided needle localization using two wires (arrowheads) to bracket this region was performed, Pathology demonstrated multiple papillomas.

Fig 2. Recurrent infiltrating ductal carcinoma in an irradiated breast in a 36-year-old woman who had undergone axinsry lymph-node dissection followed by chemotherapy 12 years earlier for presumed metastatic occult breast cancer. Mammography was negative and ultrasound examination demonstrated a suspicious mass. Breast MRI was performed to evaluate disease extent. Post-gsdolinium-DTPA fat-suppressed sagittal Tl-weighted 3D gradient-echo image demonstrates an irregular rim-enhancing mass highly suggestive of carcinoma. Pathology at ultrasound-guided core biopsy and mastectomy yielded poorly differentiated infiltrating ductal carcinoma. Note coil artifact in the inferior breast.

explained by the different pulse sequences used, threshold of suspicion based on differing diagnostic criteria, differing patient populations, and the variability in experience of the interpreting radiologists. The false-positive rate therefore depends on a variety of factors, underlining the fact that MRI must be used in the appropriate clinical setting. In clinical situations where disease prevalence is high, such as pretreatment evaluation of extent of cancer in the breast and locating occult cancer in a patient with known metastatic disease, using a test with high sensitivity is paramount. The sensitivity of breast MRI in the detection of invasive carcinomas approaches 100%. 4,15-17 By using breast MRI selectively, the high sensitivity of the examination can be exploited without generating an unacceptably high false-positive biopsy rate. False-negative cases of invasive carcinomas not detected on MRI are rare, although they can occur and are much less common than false-positive

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Fig 3. Residual tumor following attempt at breast conservation, A 65-year-old woman status post lumpectomy for two foci of infiltrating ductal carcinoma, each <1 cm, with associated ductal carcinoma in situ (DClS) and a positive margin. (A and B) Post-gadolinium-DTPA fat-suppressed sagittal T1weighted 3D gradient-echo images demonstrate residual clumped enhancement (large arrows) surrounding the seroma cavity (small arrows). Pathology at re-excision demonstrated residual DCIS.

Fig 4. Use of MRI to assess treatment response for locally advanced breast cancer. (A) Newly diagnosed inflammatory breast cancer in 9 65-year-old woman with e memmogram demonstrating uniform increased density. MRI demonstrates diffuse septal and dendritic enhancement of the breast parenchyma without focal mass. Enhancement within thickened skin indicates the inflammatory component. (B) Follow-up MR examination after five cycles of chemotherapy demonstrates near complete response with a small amount of residual tumor (arrows) in the upper breast, confirmed at mastectomy.

findings. They are so rare to be usually reportable. It appears that tumors with low cellular content, little vascularity, and high collagen content account for most of these cases. Importantly, falsenegative cases of noninvasive DCIS are not rare, as

APPROPRIATE USES OF BREAST MRI

Fig 5. Occult breast cancer metastatic to the sxilla. Mammography, screening ultrasonography, and physical examination were negative. Post-gadolinium-DTPA fat-suppressed sagittal Tl-weighted 3D gradient-echo images demonstrate an irregular mass (arrow) that proved to represent the patient's primary tumor. A second-look ultrasound study identiffed a subtle mass that underwent biopsy percutaneously yielding infiltrating ductsl carcinoma.

these lesions will exhibit an extremely variable amount of vasculadty with some lesions demonstrating angiogenesis and others not at all. The reported sensitivity of detection of DCIS ranges from 40% to 100%. 18-21 This wide variability likely reflects the variable histology of what makes up DCIS, such as degree of microinvasion, tumor grade, and size of lesion. Because false-negative cases occur with DCIS, MR/is not usually helpful in the evaluation of calcifications detected on mammography. A negative MR/result in a patient with suspicious calcifications on mammography does not obviate biopsy. 22 False-negative cases can also rarely be seen with infiltrating lobular carcinoma, as this tumor may not incite angiogenesis and it can grow in a single-file cellular arrangement. This characteristic growth pattern is likely responsible for the difficulty in the detection of infiltrating lobular carcinoma on conventional imaging. Despite the possibility of a negative MRI examination with infiltrating lobular

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carcinoma, most of this type of cancer is seen on MR/, and the extent of tumor involvement is better assessed on MRI compared with conventional imaging.23, 24 The necessity of giving intravenous contrast, the long imaging time, and restrictions on availability of scan time will limit use of M R / o f the breast. The expense of M R / a n d the variability in reimbursement also limit the clinical use of breast MR/. As with any MR/examination, claustrophobia and the presence of MR/incompatible metal devices, such as pacemakers and some aneurysm clips, preclude some patients from undergoing MR/. A theoretical limitation is the fact that there are no unified agreed on imaging parameters or protocols for breast MR/. Given the variety of magnets and imaging protocols available, it is unlikely that one single agreed on protocol will arise. Regardless, despite the variation of techniques, similar clinical indications have evolved and there is consensus on appropriate indications for MRI. Investigators in different countries operating with different patient populations and equipment have reproduced similar results with respect to high-risk screening, extent of disease evaluation, and occult tumor evaluation. The current lack of commercially available biopsy systems to fit all magnets is probably the biggest limitation in the clinical acceptance of MR/ and is discussed below. NEGATIVE PREDICTIVE VALUE

Because the sensitivity for cancer detection is high, the negative predictive value of breast MRI is high. If MRI of the breast demonstrates no enhancement and any possible technical mishap, such as intravenous contrast extravasation, has been excluded, there is an extremely high likelihood that there is no suspicious lesion. A negative MR/ examination should not deter biopsy of a suspicious lesion (BI-RADS T M [Reston, VA] 24a 4 or 5) on mammography or ultrasonography. As described, false-negative cases have been reported particularly with DCIS, and rarely with infiltrating lobular carcinoma, and well-differentiated infiltrating ctuctal carcinomas, such as medullary and tubular carcinoma. The MR/ should ideally be interpreted in conjunction with all other pertinent imaging studies, such as mammograms and ultrasounds, to arrive at the best treatment option for the patient.

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C If the MRI demonstrates no areas of enhancement and the MRI examination was technically faultless, thereby excluding any technical errors, can one assume that no invasive carcinoma is present? The answer to this question is not clear and probably depends on the clinical scenario. Because the sensitivity of MRI to DCIS is lower than with invasive carcinoma, DCIS may be present on a negative MRI examination. If the MRI examination is performed for a search of possible invasive carcinoma, such as with occult breast cancer metastatic to the axilla, a negative MRI examination virtually excludes the presence of invasive carcinoma. In our experience with patients with axillary metastases and negative MRI examinations who have not undergone surgery but have had radiation therapy, we have

,~

Fig 6. High-risk screening MR examination in a 45-year-old woman. (A and B) MR demonstrates several areas of intense enhancement that appear somewhat clumped (arrows) end are larger than punctate benign foci of enhancement. (C) MRguided needle localization of both areas revealed DCIS, solid type with negative margins. Following surgery, the patient opted for prophylactic bilateral msstectomy that demonstrated multifocal DCIS, solid type, in this breast and Iobular carcinoma in situ (LCIS) in the contralateral breast.

expectantly watched and monitored these patients carefully and in 5 years have had no cancers develop. In this patient population, the high negative predictive value of MRI potentially saves these patients from mastectomy or any other breast surgery. OUTSTANDING ISSUES Although MRI may save patients from unnecessary surgery, there is concern that findings on MRI may prompt unnecessary excess tissue removal or in some cases unnecessary mastectomy. This is particularly a concern when staging patients preoperatively. There are many questions with respect to staging that need to be answered. For example, should additional unsuspected suspicious lesions, identified only on MRI at a distance from the index

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carcinoma, necessitate excess tissue removal or a second incision or even a mastectomy? Before deciding if a patient is eligible or not for breast conservation, histologic proof of all suspicious areas on MR/ needs to be performed by either percutaneous or surgical biopsy. Otherwise, patients will be inappropriately managed and sent unnecessarily for mastectomy based on MR/findings only. M R / i s not recommended as a test to differentiate benign from malignant, except in a few cases where classic lesion morphology and enhancement is observed (Fig 7). Therefore, percutaneous biopsy of all potential suspicious areas is necessary. There is variability and choice of therapy in breast cancer. Factors that impact on the choice of surgery include tumor size, tumor grade, tumor location, and relationship of tumor size to breast size. Patient preference cannot be underestimated as psychosocial issues play an important part in the choice of therapy. Contraindications for breast conservation include multicentric disease (separate sites of tumor in different quadrants) (Fig 8) and a history of radiation. Multifocal disease (Fig 9) (separate sites of tumor in the same quadrant) can theoretically be conserved. 25

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There is evidence that radiation therapy treats subclinical disease and perhaps we are now identifying this previously undetected subclinical disease on MRI. Clearly, there will be additional foci of disease that we identify only on MRI that would have been treated successfully with radiation therapy alone. It is not known what features distinguish tumor that we can safely ignore and leave behind in the breast to be treated with radiation and what are the features of the disease that needs to be surgically excised. Is there a size limitation so that we can ignore lesions under a certain size? As a significant amount of additional disease depicted on MR/ may be DCIS, we need to know: how biologically active is DCIS found only on MRI? Unfortunately, the trials needed for the answers to these questions may never be performed because it would mean that the patients and physicians would be blinded to the MR/results. At present, if we perform an MR/ examination and identify suspicious abnormalities, we are obligated to act on this information and to presume that all suspicious abnormalities identified are clinically important. Criteria to differentiate benign and probably benign lesions, which can be followed, from suspicious lesions needing biopsy, are critical in this process and are the subject of the article on the MR lexicon elsewhere in this issue. 26 TIMING IN MENSTRUAL CYCLE

Fig 7. Classic lesion morphology seen with fibroadenoma. A Iobulated mass with nonenhancing internal septations

(curved arrow) is incidently noted on a screening examination. Background benign stippled enhancement is present.

Normal parenchyma can demonstrate enhancement that can be problematic in the interpretation of breast MR/ studies in the premenopausal patient. Areas of enhancement can appear and disappear at different phases of the menstrual cycle. Also problematic is the postmenopausal patient on hormone replacement therapy, who has parenchymal enhancement similar to that seen in the premenopausal state. Exogenous and endogenous hormones can cause increased blood flow due to a histamine-type effect. There usually is no mass effect associated with the enhancement, and kinetics of enhancement generally shows gradual increase over time. Most~ften, there will be diffuse uniform enhancement in a "stippled" fashion consisting of multiple tiny foci of enhancement that usually represent normal variant (Fig 10). Sometimes, these areas of normal parenchyma can enhance intensely and appear mass-like causing concern. 27,28

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C In general,, if possible, patients should be scheduled in the second week of their menstrual cycle when proliferative changes are at their lowest to minimize this confounding factor. If this is not possible and parenchymal enhancement is suspected, we bring the patient back in week two of a subsequent menstrual cycle for short-term followup. In the case of postmenopausal patients on

ELIZABETH A. MORRIS

B

Fig 8. Multicentric disease. Separate sites of tumor in more than one quadrant. A w woman who underwent excision of a 5-cm invssive carcinoma with positive margins. Breast MRI was performed to assess disease extent. (A and B) Multicentrir foci of DCIS in several quadrants (arrows) are shown. (C) Maximum intensity projection demonstrates the extent of disease.

hormone replacement therapy, the hormones can be stopped if necessary and a short-term follow-up in 6 to 8 weeks can be performed. LOCAL STAGING MR is able to provide important information regarding the index tumor size and the presence or absence of additional lesions as well as document-

APPROPRIATE USES OF BREAST MRI

Fig 9. Muitifocal disease. Separate sites of tumor in the same quadrant. Carcinoma identified previously in Figure 2 on a different slice demonstrates a satellite lesion (arrow) that proved to represent a second area of infiltrating ductai carcinoma.

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known preoperatively, there is a better chance of obtaining negative margins at surgery. Mapping of tumor extent by MRI is particularly helpful in difficult histologies, such as infiltrating lobular carcinoma and in tumors with an extensive intraductal component that are more often difficult to visualize on conventional imaging. It is well known that mammography underestimates the extent of DCIS, as only the calcified portions of DCIS are usually evident on the mammogram. MRI can detect uncalcified DCIS and therefore can better delineate extent in some cases (Fig 12). By better assessing tumor margins preoperatively by MRI, the return rate to the operating room for positive or close margins following lumpectomy could possibly decrease. Preoperative localization under MRI using multiple needles to map disease extent could be one way to improve margin status. Alternatively, if the tumor is solitary and MRI demonstrates that it is too large to be conserved, a recommendation of mastectomy could be offered up front to the patient following needle biopsy to prove that the tumor is malignant. In this

ing involvement of adjacent structures such as the chest wall. Tumor size and configuration are better depicted with MRI than mammography (Fig 11). Theoretically, if the extent of tumor is clearly

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Fig 10. Stippled enhancement seen in normal parenchyreal enhancement.

Fig 17. MRI delineates tumor margins with greater accuracy than mammography. A 32-year-old w o m a n with a palpable mass and 3.5 cm of pleomorphic calcifications identified on mammography. Breast MRI shows a 5.5-cm spiculated area of regional enhancement that is heterogeneous and suspicious, and more extensive than suspected on mammography. Pathology at mastectomy yielded DCIS, papillary, and cribiform types, spanning 6 cm.

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Fig 12. Extensive intraductal component delineated on MRI. A 36-year-old woman with contralateral stage I right breast cancer. (A and B) Screening MRI examination of the left breast demonstrates multiple areas of clumped linear enhancement (arrows) with an associated mass (not shown). Pathology at mastectomy yielded infiltrating ductal carcinoma with extensive intraductal component that correspond to the clumped areas on MRI.

ELIZABETH A. MORRIS

way, the patient may be spared numerous attempts at conservation. Mastectomy as initial therapy should only be recommended carefully after MRI and only after percutaneous biopsy has confirmed histologically the presence of additional lesions precluding conservation. Knowledge of multifocality and multicentricity is important to guide treatment decisions, as multicentricity will result in mastectomy whereas multifocal tumor has the potential to be conserved. In several studies, MR/ has detected other sites of tumor within the same breast in up to one third of cases. 4-6 The detection of additional sites of unsuspected tumor preoperatively could possibly improve the recurrence statistics for patients who are treated with breast conservation. Currently, the recurrence rate is 1% to 2% per year following conservation and radiation. The recurrence rate is, in part, due to under-treated disease at the time of breast conservation. If patients are identified by MRI as having a high chance of recurrence, the recurrence rate may decrease by sending these patients for more extensive surgery or mastectomy as initial therapy. Studies have also shown that MR/ is able to detect unsuspected carcinoma in the contralateral breast (Fig 13) in approximately 3% patients undergoing preoperative evaluation. 6 It appears that it may be wise to examine the contralateral breast before surgery, if bilateral examinations are not performed routinely. Evaluation of tumor spread to adjacent structures is important preoperative information for the surgeon when planning surgical approach. In large tumors, this information can be difficult to assess by either physical examination or conventional imaging with mammography or ultrasonography. MR/ offers superb visualization of the posterior breast tissue and can assess contiguous involvement better than conventional imaging (Fig 14). Invasion of the pectoralis major muscle by tumor does not alter the stage of the patient, but can affect surgical planning. If the tumor extends beyond the muscle and involves ribs, intercostal muscles, and serratus anterior muscle, then the chest wall is invaded and the staging of the patient is changed as well as the surgical therapy. 29 Knowledge of the extent of involvement of the invaded pectoralis major muscle, which presents as abnormal enhancement, can direct the surgeon intraoperatively.

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will have undergone ultrasound interrogation before MRI with a negative result. With the knowledge of the MRI results that directs the secondlook ultrasound examination, the occult primary carcinoma is often visualized. 31 MRI-GUIDED BIOPSY

Fig 13. Unsuspected contralateral carcinoma. Contralateral screening examination demonstrates a tiny irregular mass (arrow) that proved to be an incidental contralateral subcentimeter invasive carcinoma in a woman undergoing treatment for stage I breast cancer in the opposite breast.

As MRI of the breast is exquisitely sensitive and will identify lesions not seen on any other imaging modality, a method to localize and, more importantly, biopsy MRI-only depicted lesions is paramount. Although some of the larger MR-depicted lesions are identified on second-look ultrasound examination, many of the smaller lesions will only be evident on MRI. Most institutions performing biopsies use a home-built design or have modified an existing commercial device to fit their needs. 32,33 The biopsy device is loosely based on the principles of stereotactic breast biopsy with the patient prone and the breast compressed in the coil. Stereotactic breast biopsy is currently the gold standard of breast biopsy. From what we have learned, the larger the tissue sample obtained, the lower the

UNKNOWN PRIMARY MRI is the imaging modality of choice for patients presenting with axillary adenopathy positive for adenocarcinoma but negative physical examination and negative mammography. Not only can MRI identify the site of tumor (Fig 15), but it can also map extent of disease. In general, these patients are classified as at least stage II due to nodal disease. Traditionally, many often undergo mastectomy, as the site of cancer is unknown. Clearly, many patients could be conserved if unifocal or multifocal cancer is detected. For the most part, many of these tumors evade detection due to their relatively small size and the fact that they are obscured on the mammogram by dense fibroglandular tissue. The occult carcinomas typically do not contain calcifications. MRI can detect up to 86% of occult cancers in this specific clinical presentation 11,12 and can result in a lower mastectomy rate, 3~ allowing breast conservation therapy when the tumor is identified or treatment with radiation therapy alone in the event of a negative MR examination. Often after the MR examination, a second-look ultrasound examination will demonstrate the lesion that can then undergo biopsy under ultrasound guidance. Many times these patients

Fig 14. Chest wall assessment. A 60-year-old w o m a n w i t h a 6-cm palpable breast mass that is fixed to the chest wall on physical examination. Breast MRI is performed to exclude chest wall invasion. Breast MRI demonstrates that the mass abuts the chest wall though does not invade. Ribs and intercostal muscles (arrows) are not invaded.

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Fig 15. Unknown primary tumor. Occult primary breast carcinoma not detected on conventional imaging but seen on MRI as an irregular homogeneously enhancing mass (arrow) in a 50-year-old patient presenting with enlarged axillary lymph nodes biopsy positive for edenocarcinoma. Pathology yielded infiltrating ductal carcinoma.

rates of underestimation of DCIS and invasive carcinoma. Currently, tissue acquisition devices that allow large tissue sampling, such as the vacuum-assisted breast biopsy device, are not commercially available for use in the magnet. MRcompatible automated core-biopsy guns and needles are available and require further validation. Abnormalities depicted on MR can sometimes be found on second- or first-look ultrasound examination and can undergo biopsy under ultrasound guidance a potentially quicker and less espensive procedure. However, when one follows this approach, it is not always clear that the finding on MRI corresponds to the ultrasound finding. Biopsy of the lesion with the modality that best demonstrates the lesion is a general rule in breast imaging. This is particularly true when the MR-depicted lesion can be in a seemingly different location on

ELIZABETH A. MORRIS

the ultrasound examination, primarily due to the changes in patient position between the two examinations. Biopsy capability may be especially important with small foci of DCIS seen only on MRI and not on ultrasonography. Concerning MR-guided needle to localization, confirmation of specimen retrieval following needle localization is problematic, as the lesion seen only on MRI with contrast will not be seen on the x-ray specimen radiograph or on MRI once the contrast has disappeared. When performing M R localization, careful correlation of the pathologic result and the MR appearance should be made as in any case in breast imaging. In certain cases when concordance is doubtful, a postoperative MRI may assure that the lesion was appropriately removed. Close communication with the surgeon is also important so that the appropriate tissue surrounding the wire is removed. Further investigation into localizing markers that could be placed at the time of needle localization or biopsy is needed and will potentially solve this current dilemma so that lesion retrieval can be documented. CONCLUSION Breast M R / i s a powerful tool for staging breast cancer and is becoming the gold standard for the accurate staging of breast cancer before surgery. Breast M R / i s the test of choice for assessment of patients with metastatic disease to the axilla and negative mammogram and physical examination. It also plays a role in imaging the breast in identifying residual disease after lumpectomy with positive margins, and in the assessment of tumor response to adjuvant therapy. It may play a role in high-risk screening. Despite these accepted and potential uses of breast MR/, there remain many questions regarding the significance of the findings identified on MRI, particularly in the area of breast cancer staging. These questions need to be addressed by systematic involvement of breast MRI in clinical protocols.

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