REVIEW ARTICLE
Breast Magnetic Resonance Imaging Indications Stamatia Destounis, MD, FACR Abstract: The use of breast magnetic resonance imaging (MRI) has grown for the past decade and, along with the increase in use, there has been a progression in the indications for use. Breast MRI has been shown to be a valuable additional tool for breast imagers to use to provide optimal patient care. Because of the benefit that MRI can provide, the technology is now being used for a wide variety of indications, from evaluation of the extent of disease to evaluation of the high-risk patient, evaluation of tumor response to chemotherapy, and search for occult primary tumor. This review will cover the various indications for breast MRI, discuss research to date, as well as provide case examples. Key Words: breast imaging, breast MRI (Top Magn Reson Imaging 2014;23: 329–336)
F
or the past decade, magnetic resonance imaging (MRI) has been increasingly used in the field of breast imaging. This is due to the high sensitivity of up to 100%. Breast MRI was primarily used initially for evaluation of the extent of disease of recently diagnosed breast cancer; however, the applications have grown to include evaluation of the high-risk patient, assessment of response to chemotherapy, evaluation of implants, search for occult primary tumor, evaluation of suspicious discharge, and evaluation after equivocal workup. This review will provide an overview and discussion of the various indications for the use of breast MRI.
EVALUATION OF THE EXTENT OF DISEASE Evaluating the extent of disease in patients with recently diagnosed breast cancer is important for surgical planning and management (Fig. 1). The frequency of multifocal and multicentric breast cancer can vary widely, ranging from 7% to 63%.1–4 The American College of Radiology (ACR) as well as the American Cancer Society (ACS) and the Society of Breast Imaging (SBI) support MRI utilization for the evaluation of the extent of disease. The ACR guidance document stated that MRI determines the extent of disease more accurately than standard mammography and physical examination in many patients.5 In addition to evaluating the ipsilateral breast after a breast cancer diagnosis, MRI has shown benefit in evaluating the contralateral breast. Studies have demonstrated that MRI can detect contralateral breast cancers that were otherwise occult in an average of 5% of women with a recent diagnosis of breast cancer.6–10 A landmark study by Lehman et al9 found that MRI was able to detect cancers that were occult to mammography and clinical examination in 30 of 969 women who were already diagnosed with breast cancer in 1 breast. Magnetic resonance imaging was shown to improve detection in the contralateral breast while maintaining a false-positive rate of 10.9%. All of the cancers detected through MRI in the study of Lehman et al9 were node negative and 40% were ductal carcinoma in situ (DCIS). The authors discussed the importance of the findings From the Elizabeth Wende Breast Care, LLC, Rochester, NY. Reprints: Stamatia Destounis, MD, FACR, Elizabeth Wende Breast Care, LLC, 170 Sawgrass Dr, Rochester, NY 14620 (e‐mail: [email protected]). The author declares no conflict of interest. Copyright ©2014 by Lippincott Williams & Wilkins
because the success of a modality to be used as a screening tool is directly related to the ability to detect early cancers. The use of MRI for the detection of DCIS has been disputed for years because some have argued that MRI evaluation of DCIS is not beneficial. However, studies have also found that MRI can help to improve the diagnosis of DCIS (Fig. 2). Kuhl et al11 investigated 193 women with pure DCIS; mammography detected 93 (56%) DCIS, whereas MRI was able to detect 153 (92%) DCIS. Specifically, mammography missed 43 cases of highgrade DCIS; all of which were detected using MRI. Contrary to this, a study of 98 patients with DCIS found that MRI does not accurately predict the extent of disease in patients with extensive DCIS, although in patients with MRI tumor size of less than or equal to 2 cm, it may assist with surgical planning.12 The authors cautioned that the decision to refer a patient to mastectomy should not be made on the MRI findings alone. The use of breast MRI for the evaluation of the extent of disease has been challenged because some argue that it remains to be proven that the increased accuracy results in a reduction in recurrence rates after surgery, radiation, or systemic therapy. A recent study by Houssami et al13 evaluated the association between preoperative MRI as well as local and distant recurrence in patients diagnosed with breast cancer and concluded that performing MRI preoperatively was not found to reduce local or distant recurrence risks. Despite the arguments for and against the use of MRI presurgically, breast MRI is helpful to evaluate ipsilateral and contralateral disease in patients with a recent breast cancer diagnosis.
EVALUATION OF THE HIGH-RISK PATIENT Magnetic resonance imaging evaluation of the high-risk patient consists of patients with personal and/or family history of breast cancer, genetic predisposition, history of biopsy-proven atypia (lobular carcinoma in situ, atypical lobular hyperplasia, atypical ductal hyperplasia, radial scar), or prior mantle radiation for Hodgkin disease. Breast MRI may specifically be indicated in the surveillance of women with more than 20% lifetime risk for breast cancer.5 Societies such as the ACR, the SBI, and the ACS recommend the use of MRI screening for these high-risk populations. The ACR recommendations stated that patients should be referred for MRI screening after risk assessment or counseling has been performed by trained personnel or by their referring physician who used a risk assessment model.5 The ACS specifically recommends annual MRI for women who have a lifetime risk of 20% to 25% or greater according to risk assessment models, have a known BRCA1 or BRCA2 gene mutation (Fig. 3), have a first-degree relative with BRCA1 or BRCA2 mutation and have not had testing themselves, had radiation to the chest wall between ages 10 and 30 years, or personal or first-degree family history of Li-Fraumeni syndrome, Cowden syndrome, or Bannayan-Riley-Ruvalcaba syndrome.14 The ACS recommends against MRI screening for those with lifetime risk of less than 15%. Further, the ACS does not make a recommendation for or against annual MRI screening for women at moderate risk (15%–20%), those with personal history of atypia, or those with dense breasts. Screening these patients
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
www.topicsinmri.com
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
329
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
Destounis
FIGURE 1. A–D, A 71-year-old patient presented for MRI evaluation after recent diagnosis of the left breast IDC (A–B). Breast MRI (C–D) revealed multiple satellite-enhancing masses throughout the left breast.
should be determined on a case-by-case basis. Both the ACR and the SBI endorse the ACS recommendations. Studies have demonstrated that breast MRI can significantly improve the detection of cancer that is otherwise clinically, mammographically, and sonographically occult.9,15–22 Such research has led to a dramatic increase in the use of screening breast MRI for the high-risk patient. Our facility has experienced this increase in utilization because we have seen an increase from 36% in 2008, which was our first year of breast MRI being available daily at our facility, to 61% in 2011. Morris et al18 published one study, which reviewed the records of 367 women at high risk for developing breast cancer who had normal mammographic findings. The patients' first breast MRI screening examination was within a 2-year period. On the basis of MRI, biopsy was recommended in 17% of the patients, with carcinoma identified in 24% of those who underwent biopsy or 4% of women who had breast MRI screening. The positive predictive value of biopsy based on MRI findings in the study was significantly greater in women with a family history of breast cancer (32%), particularly among those women who had both a family history and a personal history of breast cancer (50%). Similarly, Lehman et al17 conducted a large prospective study evaluating genetically high-risk women. The patients were screened with both mammography and breast MRI. Four cancers were ultimately detected; all were identified through MRI and 1 cancer was identified through mammography. Twenty-three (6.3%) women were recommended for biopsy with a resultant positive predictive value of 17%. The benefit of added cancer yield in the study was associated with a higher false-positive rate for MRI compared with mammography, which was similar to previous studies. When specifically reviewing patients with a personal history of breast cancer, it has been reported that breast MRI can detect
330
www.topicsinmri.com
recurrence as well as differentiate recurrence from postsurgical changes23 (Fig. 4). This is important because it has been reported that 18% of conservatively treated invasive breast cancers will have local recurrence within 10 years of treatment, most within 5 years, with local recurrence rates ranging from 4.3% to 10%.24 The rate of local recurrence at the chest wall after mastectomy has been reported to range between 5% and 27%, with approximately 80% of local recurrences occurring within the first 5 years; 25% to 35% of local recurrences cause significant morbidity.23 Studies have demonstrated that, among high-risk women who have breast MRI screening, 3% to 15% have a subsequent biopsy resulting in benign findings.25–27 The lower specificity of breast MRI does lead to a large number of benign biopsies; one reason that the technology is not applied as a screening modality for the general population. Despite this, breast MRI screening can aid in the detection of early-stage (small and node-negative) cancers in the high-risk population.15 Guidance from the ACS, the ACR, and the SBI provides support for screening specific high-risk populations.
ASSESSMENT OF RESPONSE TO CHEMOTHERAPY Magnetic resonance imaging has the ability to differentiate between nonvascularized therapy-induced fibrosis and residual tumor. It is the thought that this can allow for the ability to identify tumors not responding to treatment and potentially predict presence of residual tumors after neoadjuvant chemotherapy. This could ultimately impact surgical management of the patient. Breast MRI evaluation can be incorporated in the management of a patient during treatment as well as after treatment has concluded. It has been reported that MRI can provide evidence of response to therapy 6 weeks after the start of chemotherapy treatment.28 Overall, there is agreement in the literature that ©2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
Breast MRI Indications
FIGURE 2. A–D, A 45-year-old patient presented for MRI evaluation of the extent of disease after a diagnosis of the left breast DCIS measuring 1.2 cm. Mammography examination was negative (A–B); carcinoma was detected on ultrasound (C). Magnetic resonance imaging revealed extensive linear, irregular enhancement in the left breast (D). Magnetic resonance imaging findings altered the patient's management from lumpectomy to mastectomy. At surgical excision, pathology revealed IDC with DCIS measuring 2.8 cm.
MRI is a valuable method for the assessment of tumor response after chemotherapy; however, there are differing opinions regarding the accuracy of MRI at precisely measuring the size of the residual tumor.29 Rieber et al27 found that MRI is helpful in
monitoring response; however, it can be unreliable for determining the size of residual tumor in patients having a significant response to the chemotherapy treatment, finding that MRI often underestimated the amount of residual tumor.28 Other studies have
FIGURE 3. A–B, A 42-year-old unaffected patient presented for breast MRI screening after genetic testing revealed a deleterious mutation in the BRCA1 gene. High-risk MRI detected an enhancing mass in the right breast (A). Targeted ultrasound (B) identified the mass and ultrasound-guided biopsy was performed, resulting in a diagnosis of IDC. ©2014 Lippincott Williams & Wilkins
www.topicsinmri.com
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
331
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
Destounis
FIGURE 4. A–D, Patient presented for MRI evaluation of scar from prior left lumpectomy. Recent mammographic imaging (A–B) demonstrated an area of asymmetry near the scar, which partially resolved on a magnification view (C). Magnetic resonance imaging identified an enhancing mass (D) and MRI biopsy was performed, resulting in a diagnosis of IDC.
FIGURE 5. A–B, A 46-year-old patient presented for MRI evaluation after 7 cycles of chemotherapy treatment. The patient was diagnosed with a 2.3-cm right breast IDC with metastases to lymph nodes (A). On posttreatment MRI (B), previously seen lymphadenopathy was no longer present and the site of IDC was no longer enhanced, with reduction in size to 8 mm. At surgical excision, IDC measured 2.0 cm, with 2 of the 21 lymph nodes positive for metastatic disease, demonstrating that MRI underestimated the size of the residual tumor.
332
www.topicsinmri.com
©2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
Breast MRI Indications
FIGURE 6. A–D, A patient presented for MRI evaluation after presenting for evaluation of right bloody nipple discharge. Mammographic and sonographic images were negative (A–B). An attempt was made at ductography but was unsuccessful because of contrast extravasation. Slides of the discharge were hemoccult positive. Magnetic resonance imaging detected abnormal ductal enhancement from the nipple posteriorly (C–D). Pathology at surgical excision revealed extensive DCIS.
reported high correlation between MRI and histology.29–31 On the basis of the literature, MRI has shown to be accurate in identifying cancers in nonresponders and those with partial response to treatment; however, MRI tends to underestimate the size of tumors that have a good response to treatment.32 Orel33 stated that this is likely related to chemotherapy-induced decrease in tumor vascularization and decreased vascular permeability. It is also thought that the ability of MRI to detect residual tumor may be dependent on the chemotherapeutic agent used; the use of taxane-containing regimens has been associated with underestimation of residual tumor on MRI.34 As stated by Orel,33 the use of breast MRI to evaluate tumor response after chemotherapy is the most accurate imaging method, although it is important to be
mindful of the potential for the tumor to be overestimated or underestimated (Fig. 5).
MRI DETECTION OF OCCULT PRIMARY TUMOR Patients with axillary lymph node metastases consistent with breast origin and patients with distant metastases suggestive of primary breast cancer can be management dilemmas for the breast imager. Occult breast cancer in patients presenting with isolated axillary lymph nodes without a known breast cancer represents up to 1% of operable breast cancer.35–37 Published reports on the use of MRI to evaluate occult primary breast cancer have had similar findings.38,39 A small study conducted by Olson et al37
FIGURE 7. A–B, A 48-year-old patient presented for MRI evaluation of bilateral silicone implants because of suspicion of implant leak. Imaging of the right breast (A–B) revealed that portions of the implant wall folded, suggestive of intracapsular implant rupture. ©2014 Lippincott Williams & Wilkins
www.topicsinmri.com
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
333
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
Destounis
FIGURE 8. A–D, A patient presented for diagnostic evaluation of slight skin puckering of the right breast. Mammogram and ultrasound were equivocal (A–B), with suspicious physical examination findings. Bilateral MRI was performed for evaluation of inconclusive workup and revealed a 3.8-cm area of regional enhancement from the subareolar region posteriorly (C–D). Targeted ultrasound and ultrasound-guided biopsy were performed for a diagnosis of invasive mammary carcinoma.
found that MRI identified a primary breast cancer in 70% of patients included in the study. These patients were women with a biopsy-proven metastatic adenocarcinoma to an axillary lymph node without evidence of primary breast cancer. In addition, Lu et al38 performed a similar study reviewing 35 women with occult breast cancer. The study found that MRI revealed primary breast cancer in 21 of the 35 patients. Small mass lesions and lesions with ductal or segmental enhancement were found to be common features in patients with occult breast cancer and the predominant type of histology was invasive ductal carcinoma (IDC) of moderate grade. The authors also noted that the rate of triplenegative breast cancer may be higher in cases of occult breast cancer. Stomper et al39 performed a small analysis of 8 patients and found that breast MRI can identify the primary tumor site and influence management of patients presenting with clinically and mammographically occult primary breast carcinomas. The use of breast MRI is indicated when evaluating axillary metastases with unknown primary tumor.
EVALUATION OF SUSPICIOUS DISCHARGE It has been reported that the incidence of malignancy in patients presenting with discharge ranges from 5% to 20%.40 There
334
www.topicsinmri.com
is benefit from imaging with mammography, ultrasound, and galactography/ductography. However, there are cases where further evaluation is required (Fig. 6). Traditionally, when clinical evaluation was negative, major duct excision would be the next step for the patient. However, although research on the use of MRI in the evaluation of discharge is somewhat limited, there have been promising findings because the technology has proven its ability to detect otherwise occult breast cancer. A study by Tokuda et al41 evaluated 47 patients with suspicious nipple discharge with MRI and found that MRI was able to provide clinically useful information. Further, Ballesio et al42 found when evaluating 44 patients with discharge and negative mammographic findings that MRI was able to diagnose ductal disease. Similarly, Nakahara et al43 reported that MRI was able to detect all malignancies in the study cohort. Facilities may find that breast MRI is a beneficial option, especially when galactography/ductography is not available.
EVALUATION OF IMPLANT INTEGRITY According to the ACR guidelines, breast MRI may be indicated for evaluating patients with implants.5 The ACS stated that, when performing breast MRI to evaluate silicone implants, a noncontrast MRI can be used, whereas contrast MRI can aid ©2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
in the evaluation of silicone, saline, and/or free injections with silicone, paraffin, or polyacrylamide gel. Findings on MRI representing implant rupture include intracapsular findings (keyhole appearance, subcapsular line, and linguine sign) and extracapsular findings (extracapsular rupture). Studies have shown that MRI is more sensitive for the detection of implant rupture than other imaging methods (Fig. 7). Everson et al44 compared findings of mammography, sonography, computed tomography, and MRI as well as determined that MRI was more sensitive and specific for detecting implant rupture. Similarly, a study by Di Benedetto et al45 found a sensitivity of 93% and a specificity of 73% for MRI compared with 68% and 81% for mammography as well as 77% and 69% for ultrasound, respectively. This study found that mammography and ultrasound were very specific for the detection of extracapsular rupture, whereas overall MRI was the most sensitive for the detection of implant rupture. Breast MRI is an effective imaging method when there is suspicion of an implant rupture.
MRI EVALUATION AFTER INCONCLUSIVE WORKUP Because of the high sensitivity of MRI, the technology can be used to problem solve after equivocal imaging findings with mammography, ultrasound, and physical examination (Fig. 8). It has been suggested that, when there is a negative MRI when evaluating inconclusive workup, the presence of invasive cancer is excluded.46 Although, there are also reports documenting the false-negative rates of MRI from 4% to 12%.47–50 Lee et al50 evaluated the usefulness of MRI for the evaluation of equivocal mammography cases and found that MRI was helpful as an adjunct to evaluate these cases. Magnetic resonance imaging was able to help determine the need for biopsy and, in doing so, was able to diagnose malignancies that might otherwise have been undiagnosed. Further, a negative MRI allowed for surveillance through mammography rather than biopsy. The use of MRI in the setting of equivocal workup with mammography and ultrasound is beneficial, although it is important to not replace the standard imaging workup with MRI. It is important to keep in mind the average specificity of the technology, which does lead to an increased number of false-positive findings and biopsies performed.
MRI-GUIDED BIOPSY Breast MRI performed for any indication can identify suspicious findings that are not detected through mammography, ultrasound, or physical examination. Because of this, a method to biopsy MRI-only lesions is necessary. It is helpful to use targeted ultrasound as the first step after a lesion is identified on MRI. However, targeted ultrasound can fail to identify these MRI-detected lesions in up to 77%,51 although it has also been reported that targeted ultrasound has the ability to identify a correlate in up to 70%.52 In cases where the lesion is not demonstrated on targeted ultrasound, MRI biopsy is indicated. Studies have proven that MRI-guided biopsy is a fast and reliable alternative to surgical excision.53–56 Nonvisualization of lesions at MRI biopsy can occur and has been reported to occur in up to 13%.56 In cases such as these, it is important to perform short-term follow-up to ensure stability. When a facility performs breast MRI, a method to accurately sample MRI-only lesions is vital.
Breast MRI Indications
continue to advance. Breast MRI has proven its benefit in evaluating patients with a recent breast cancer diagnosis as well as patients at high risk for the development of breast cancer. Breast imaging facilities will have to continue to evaluate and reassess the indications following the current guidelines for breast MRI and the evolving needs of the patients.
REFERENCES 1. Holland R, Veling S, Mravunac M, et al. Histologic multifocality of Tis, T1-2 breast carcinomas. Implications for clinical trials of breast-conserving surgery. Cancer. 1985;56:979–990. 2. Anastassiades O, Iakovou E, Stavridou N, et al. Multicentricity in breast cancer. A study of 366 cases. Am J Clin Pathol. 1993;99:238–243. 3. Schwartz G, Patchesfsky A, Feig S, et al. Multicentricity of non-palpable breast cancer. Cancer. 1980;45:2913–2916. 4. Vaidya J, Vyas J, Chinoy R, et al. Multicentricity of breast cancer: whole-organ analysis and clinical implications. Br J Cancer. 1996;74: 820–824. 5. ACR Practice Guideline for the Performance of Contrast-Enhanced Magnetic Resonance Imaging (MRI) of the Breast. http://www.acr.org/ Quality-Saftey/Standards-Guidelines-by-Modality/MRI. Accessed February 18, 2014. 6. Lehman CD, Gatsonis C, Kuhl CK, et al. MRI evaluation of the contralateral breast in women with recently diagnosed breast cancer. N Engl J Med. 2007;356:1295–1303. 7. Fischer U, Kopka L, Grabbe E. Breast carcinoma: effect of preoperative contrast-enhanced MR imaging on the therapeutic approach. Radiology. 1999;213:881–888. 8. Kuhl C, Schmiedel A, Morakkabiti N. Breast MR imaging of the asymptomatic contralateral breast in the work-up or follow-up of patients with unilateral breast cancer. Radiology. 2000;217:268. 9. Lee SG, Orel SG, Woo IJ, et al. MR imaging screening of the contralateral breast in patients with newly diagnosed breast cancer: preliminary results. Radiology. 2003;226:773–778. 10. Liberman L, Morris EA, Kim CM, et al. MR imaging findings in the contralateral breast of women with recently diagnosed breast cancer. AJR Am J Roentgenol. 2003;180:333–341. 11. Kuhl CK, Schrading S, Bieling HB, et al. MRI for diagnosis of pure ductal carcinoma in situ: a prospective observational study. Lancet. 2007;370: 485–492. 12. Allen LR, Lago-Toro CE, Hughes JH, et al. Is there a role for MRI in the preoperative assessment of patients with DCIS? Ann Surg Oncol. 2010;17:2395–2400. 13. Houssami N, Turner R, Macaskill P, et al. An individual person data meta-analysis of preoperative magnetic resonance imaging and breast cancer recurrence. J Clin Oncol. 2014;32:392–401. 14. Saslow D, Boetes C, Burke W, et al. American Cancer Society guidelines for breast screening with MRI as an adjunct to mammography. CA Cancer J Clin. 2007;57:75–89. 15. Kriege M, Brekelmans CT, Boetes C, et al. Efficacy of MRI and mammography for breast-cancer screening in women with a familial or genetic predisposition. N Engl J Med. 2004;351:427–437. 16. Kuhl C, Weigel S, Schrading S, et al. Prospective multicenter cohort study to refine management recommendations for women at elevated familial risk of breast cancer: the EVA trial. J Clin Oncol. 2010;28:1450–1457.
CONCLUSIONS
17. Lehman CD, Blume JD, Weatherall P, et al. Screening women at high risk for breast cancer with mammography and magnetic resonance imaging. Cancer. 2005;103:1898–1905.
The use of breast MRI has evolved for the last decade. As radiologists continue to evaluate the technology, the role will
18. Morris EA, Liberman L, Ballon DJ, et al. MRI of occult breast carcinoma in a high-risk population. AJR Am J Roentgenol. 2003;181:619–626.
©2014 Lippincott Williams & Wilkins
www.topicsinmri.com
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
335
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
Destounis
19. Sardanelli F, Podo F, Santoro F, et al. Multicenter surveillance of women at high genetic breast cancer risk using mammography, ultrasonography, and contrast-enhanced magnetic resonance imaging (the high breast cancer risk Italian 1 study): final results. Invest Radiol. 2011;46:94–105. 20. Warner E, Plewes DB, Hill KA, et al. Surveillance of BRCA1 and BRCA2 mutation carriers with magnetic resonance imaging, ultrasound, mammography, and clinical breast examination. JAMA. 2004;292: 1317–1325. 21. Berg WA, Zhang Z, Lehrer D, et al. Detection of breast cancer with addition of annual screening ultrasound or a single screening MRI to mammography in women with elevated breast cancer risk. JAMA. 2012;307:1394–1404. 22. Yilmaz MH, Esen G, Ayarcan Y, et al. The role of US and MR imaging in detecting local chest wall tumor recurrence after mastectomy. Diagn Interv Radiol. 2007;13:13–18. 23. Davis PL, McCarty KS Jr. Sensitivity of enhanced MRI for the detection of breast cancer: new, multicentric, residual, and recurrent. Eur Radiol. 1997;7:S289–S298. 24. Kuhl CK, Schmutzler RK, Leutner CC, et al. Breast MR imaging screening in 192 women proved or suspected to be carriers of a breast cancer susceptibility gene: preliminary results. Radiology. 2000;215:267–279. 25. Warner E, Plewes DB, Shumak RS, et al. Comparison of breast magnetic resonance imaging, mammography, and ultrasound for surveillance of women at high risk for hereditary breast cancer. J Clin Oncol. 2001;19:3521–3531. 26. Stoutjesdijk MJ, Boetes C, Jager GJ, et al. Magnetic resonance imaging and mammography in women with a hereditary risk of breast cancer. J Natl Cancer Inst. 2001;93:1095–1102. 27. Rieber A, Brambs HJ, Gabelmann A, et al. Breast MRI for monitoring response of primary breast cancer to neo-adjuvant chemotherapy. Eur Radiol. 2002;12:1711–1719. 28. Rosen EL, Blackwell KL, Baker JA, et al. Accuracy of MRI in the detection of residual breast cancer after neoadjuvant chemotherapy. AJR Am J Roentgenol. 2003;181:1275–1282. 29. Weatherall PT, Evans GF, Metzger GJ, et al. MRI vs. histologic measurement of breast cancer following chemotherapy: comparison with x-ray mammography and palpation. J Magn Reson Imaging. 2001;13:868–875. 30. Partridge SC, Gibbs JE, Lu Y, et al. Accuracy of MR imaging for revealing residual breast cancer in patients who have undergone neoadjuvant chemotherapy. AJR Am J Roentgenol. 2002;179:1193–1199. 31. Yeh E, Slanetz P, Kopans DB, et al. Prospective comparison of mammography, sonography, and MRI in patients undergoing neoadjuvant chemotherapy for palpable breast cancer. AJR Am J Roentgenol. 2005;184:868–877. 32. Denis F, Desbiez-Bourcier AV, Chapiron C, et al. Contrast enhanced magnetic resonance imaging underestimates residual disease following neoadjuvant docetaxel based chemotherapy for breast cancer. Eur J Surg Oncol. 2004;30:1069–1076. 33. Orel S. Who should have breast magnetic resonance imaging evaluation? J Clin Oncol. 2008;26:703–711. 34. Baron PL, Moore MP, Kinne DW, et al. Occult breast cancer presenting with axillary metastases. Updated management. Arch Surg. 1990;125:210–214. 35. Copeland EM, McBride CM. Axillary metastases from unknown primary sites. Ann Surg. 1973;178:25–27. 36. Rosen PP. Axillary lymph node metastases in patients with occult noninvasive breast carcinoma. Cancer. 1980;46:1298–1306.
336
www.topicsinmri.com
37. Olson JA Jr, Morris EA, Van Zee KJ, et al. Magnetic resonance imaging facilitates breast conservation for occult breast cancer. Ann Surg Oncol. 2000;7:411–415. 38. Lu H, Xu YL, Zhang SP, et al. Breast magnetic resonance imaging in patients with occult breast carcinoma: evaluation on feasibility and correlation with histopathological findings. Chin Med J (Engl). 2011;124: 1790–1795. 39. Stomper PC, Waddell BE, Edge SB, et al. Breast MRI in the evaluation of patients with occult primary breast carcinoma. Breast J. 1999;5:230–234. 40. Tjalma W, Verslegers I. Nipple discharge and the value of MR imaging. Eur J Obstet Gynecol Reprod Biol. 2004;115:234–236. 41. Tokuda Y, Kuriyama K, Nakamoto A, et al. Evaluation of suspicious nipple discharge by magnetic resonance mammography based on breast imaging reporting and data system magnetic resonance imaging descriptors. J Comput Assist Tomogr. 2009;33:58–62. 42. Ballesio L, Maggi C, Savelli S, et al. Role of breast magnetic resonance imaging (MRI) in patients with unilateral nipple discharge: preliminary study. Radiol Med. 2008;113:249–264. 43. Nakahara H, Namba K, Watanabe R, et al. A comparison of MR imaging, galactography and ultrasonography in patients with nipple discharge. Breast Cancer. 2003;10:320–329. 44. Everson LI, Parantainen H, Detlie T, et al. Diagnosis of breast implant rupture: imaging findings and relative efficacies of imaging techniques. AJR Am J Roentgenol. 1994;163:57–60. 45. Di Benedetto G, Cecchini S, Grassetti L, et al. Comparative study of breast implant rupture using mammography, sonography, and magnetic resonance imaging: correlation with surgical findings. Breast J. 2008;14:532–537. 46. Kelcz F, Santyr G. Gadolinium-enhanced breast MRI. Crit Rev Diagn Imaging. 1995;36:287–338. 47. Ghai S, Muradali D, Bukhanov K, et al. Nonenhancing breast malignancies on MRI: sonographic and pathologic correlation. AJR Am J Roentgenol. 2005;185:481–419. 48. Boetes C, Strijk SP, Holland R, et al. False-negative MR imaging of malignant breast tumors. Eur Radiol. 1997;7:1231–1234. 49. Teifke A, Hlawatsch A, Beier T, et al. Undetected malignancies of the breast: dynamic contrast-enhanced MR imaging at 1.0 T. Radiology. 2002; 224:881–888. 50. Lee CH, Smith RC, Levine JA, et al. Clinical usefulness of MR imaging of the breast in the evaluation of the problematic mammogram. AJR Am J Roentgenol. 1999;173:1323–1329. 51. LaTrenta LR, Menell JH, Morris EA, et al. Breast lesions detected with MR imaging: utility and histopathologic importance of identification with US. Radiology. 2003;227:856–861. 52. Destounis S, Arieno A, Somerville PA, et al. Community-based practice experience of unsuspected breast magnetic resonance imaging abnormalities evaluated with second-look sonography. J Ultrasound Med. 2009;28:1337–1346. 53. Liberman L, Morris EA, Dershaw DD, et al. Fast MRI-guided vacuum-assisted breast biopsy: initial experience. AJR Am J Roentgenol. 2003;181:1283–1293. 54. Liberman L, Bracero N, Morris E, et al. MRI-guided 9-gauge vacuum-assisted breast biopsy: initial clinical experience. AJR Am J Roentgenol. 2005;185:183–183. 55. Lehman C, DePeri ER, Peacock S, et al. Clinical experience with MRI-guided vacuum-assisted breast biopsy. AJR Am J Roentgenol. 2005;182:48. 56. Perlet C, Heinig A, Prat X, et al. Multicenter study for the evaluation of a dedicated biopsy device for MR-guided vacuum biopsy of the breast. Eur Radiol. 2002;12:1463–1470.
©2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Breast Magnetic Resonance Imaging Indications Stamatia Destounis, MD, FACR Abstract: The use of breast magnetic resonance imaging (MRI) has grown for the past decade and, along with the increase in use, there has been a progression in the indications for use. Breast MRI has been shown to be a valuable additional tool for breast imagers to use to provide optimal patient care. Because of the benefit that MRI can provide, the technology is now being used for a wide variety of indications, from evaluation of the extent of disease to evaluation of the high-risk patient, evaluation of tumor response to chemotherapy, and search for occult primary tumor. This review will cover the various indications for breast MRI, discuss research to date, as well as provide case examples. Key Words: breast imaging, breast MRI (Top Magn Reson Imaging 2014;23: 329–336)
F
or the past decade, magnetic resonance imaging (MRI) has been increasingly used in the field of breast imaging. This is due to the high sensitivity of up to 100%. Breast MRI was primarily used initially for evaluation of the extent of disease of recently diagnosed breast cancer; however, the applications have grown to include evaluation of the high-risk patient, assessment of response to chemotherapy, evaluation of implants, search for occult primary tumor, evaluation of suspicious discharge, and evaluation after equivocal workup. This review will provide an overview and discussion of the various indications for the use of breast MRI.
EVALUATION OF THE EXTENT OF DISEASE Evaluating the extent of disease in patients with recently diagnosed breast cancer is important for surgical planning and management (Fig. 1). The frequency of multifocal and multicentric breast cancer can vary widely, ranging from 7% to 63%.1–4 The American College of Radiology (ACR) as well as the American Cancer Society (ACS) and the Society of Breast Imaging (SBI) support MRI utilization for the evaluation of the extent of disease. The ACR guidance document stated that MRI determines the extent of disease more accurately than standard mammography and physical examination in many patients.5 In addition to evaluating the ipsilateral breast after a breast cancer diagnosis, MRI has shown benefit in evaluating the contralateral breast. Studies have demonstrated that MRI can detect contralateral breast cancers that were otherwise occult in an average of 5% of women with a recent diagnosis of breast cancer.6–10 A landmark study by Lehman et al9 found that MRI was able to detect cancers that were occult to mammography and clinical examination in 30 of 969 women who were already diagnosed with breast cancer in 1 breast. Magnetic resonance imaging was shown to improve detection in the contralateral breast while maintaining a false-positive rate of 10.9%. All of the cancers detected through MRI in the study of Lehman et al9 were node negative and 40% were ductal carcinoma in situ (DCIS). The authors discussed the importance of the findings From the Elizabeth Wende Breast Care, LLC, Rochester, NY. Reprints: Stamatia Destounis, MD, FACR, Elizabeth Wende Breast Care, LLC, 170 Sawgrass Dr, Rochester, NY 14620 (e‐mail: [email protected]). The author declares no conflict of interest. Copyright ©2014 by Lippincott Williams & Wilkins
because the success of a modality to be used as a screening tool is directly related to the ability to detect early cancers. The use of MRI for the detection of DCIS has been disputed for years because some have argued that MRI evaluation of DCIS is not beneficial. However, studies have also found that MRI can help to improve the diagnosis of DCIS (Fig. 2). Kuhl et al11 investigated 193 women with pure DCIS; mammography detected 93 (56%) DCIS, whereas MRI was able to detect 153 (92%) DCIS. Specifically, mammography missed 43 cases of highgrade DCIS; all of which were detected using MRI. Contrary to this, a study of 98 patients with DCIS found that MRI does not accurately predict the extent of disease in patients with extensive DCIS, although in patients with MRI tumor size of less than or equal to 2 cm, it may assist with surgical planning.12 The authors cautioned that the decision to refer a patient to mastectomy should not be made on the MRI findings alone. The use of breast MRI for the evaluation of the extent of disease has been challenged because some argue that it remains to be proven that the increased accuracy results in a reduction in recurrence rates after surgery, radiation, or systemic therapy. A recent study by Houssami et al13 evaluated the association between preoperative MRI as well as local and distant recurrence in patients diagnosed with breast cancer and concluded that performing MRI preoperatively was not found to reduce local or distant recurrence risks. Despite the arguments for and against the use of MRI presurgically, breast MRI is helpful to evaluate ipsilateral and contralateral disease in patients with a recent breast cancer diagnosis.
EVALUATION OF THE HIGH-RISK PATIENT Magnetic resonance imaging evaluation of the high-risk patient consists of patients with personal and/or family history of breast cancer, genetic predisposition, history of biopsy-proven atypia (lobular carcinoma in situ, atypical lobular hyperplasia, atypical ductal hyperplasia, radial scar), or prior mantle radiation for Hodgkin disease. Breast MRI may specifically be indicated in the surveillance of women with more than 20% lifetime risk for breast cancer.5 Societies such as the ACR, the SBI, and the ACS recommend the use of MRI screening for these high-risk populations. The ACR recommendations stated that patients should be referred for MRI screening after risk assessment or counseling has been performed by trained personnel or by their referring physician who used a risk assessment model.5 The ACS specifically recommends annual MRI for women who have a lifetime risk of 20% to 25% or greater according to risk assessment models, have a known BRCA1 or BRCA2 gene mutation (Fig. 3), have a first-degree relative with BRCA1 or BRCA2 mutation and have not had testing themselves, had radiation to the chest wall between ages 10 and 30 years, or personal or first-degree family history of Li-Fraumeni syndrome, Cowden syndrome, or Bannayan-Riley-Ruvalcaba syndrome.14 The ACS recommends against MRI screening for those with lifetime risk of less than 15%. Further, the ACS does not make a recommendation for or against annual MRI screening for women at moderate risk (15%–20%), those with personal history of atypia, or those with dense breasts. Screening these patients
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
www.topicsinmri.com
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
329
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
Destounis
FIGURE 1. A–D, A 71-year-old patient presented for MRI evaluation after recent diagnosis of the left breast IDC (A–B). Breast MRI (C–D) revealed multiple satellite-enhancing masses throughout the left breast.
should be determined on a case-by-case basis. Both the ACR and the SBI endorse the ACS recommendations. Studies have demonstrated that breast MRI can significantly improve the detection of cancer that is otherwise clinically, mammographically, and sonographically occult.9,15–22 Such research has led to a dramatic increase in the use of screening breast MRI for the high-risk patient. Our facility has experienced this increase in utilization because we have seen an increase from 36% in 2008, which was our first year of breast MRI being available daily at our facility, to 61% in 2011. Morris et al18 published one study, which reviewed the records of 367 women at high risk for developing breast cancer who had normal mammographic findings. The patients' first breast MRI screening examination was within a 2-year period. On the basis of MRI, biopsy was recommended in 17% of the patients, with carcinoma identified in 24% of those who underwent biopsy or 4% of women who had breast MRI screening. The positive predictive value of biopsy based on MRI findings in the study was significantly greater in women with a family history of breast cancer (32%), particularly among those women who had both a family history and a personal history of breast cancer (50%). Similarly, Lehman et al17 conducted a large prospective study evaluating genetically high-risk women. The patients were screened with both mammography and breast MRI. Four cancers were ultimately detected; all were identified through MRI and 1 cancer was identified through mammography. Twenty-three (6.3%) women were recommended for biopsy with a resultant positive predictive value of 17%. The benefit of added cancer yield in the study was associated with a higher false-positive rate for MRI compared with mammography, which was similar to previous studies. When specifically reviewing patients with a personal history of breast cancer, it has been reported that breast MRI can detect
330
www.topicsinmri.com
recurrence as well as differentiate recurrence from postsurgical changes23 (Fig. 4). This is important because it has been reported that 18% of conservatively treated invasive breast cancers will have local recurrence within 10 years of treatment, most within 5 years, with local recurrence rates ranging from 4.3% to 10%.24 The rate of local recurrence at the chest wall after mastectomy has been reported to range between 5% and 27%, with approximately 80% of local recurrences occurring within the first 5 years; 25% to 35% of local recurrences cause significant morbidity.23 Studies have demonstrated that, among high-risk women who have breast MRI screening, 3% to 15% have a subsequent biopsy resulting in benign findings.25–27 The lower specificity of breast MRI does lead to a large number of benign biopsies; one reason that the technology is not applied as a screening modality for the general population. Despite this, breast MRI screening can aid in the detection of early-stage (small and node-negative) cancers in the high-risk population.15 Guidance from the ACS, the ACR, and the SBI provides support for screening specific high-risk populations.
ASSESSMENT OF RESPONSE TO CHEMOTHERAPY Magnetic resonance imaging has the ability to differentiate between nonvascularized therapy-induced fibrosis and residual tumor. It is the thought that this can allow for the ability to identify tumors not responding to treatment and potentially predict presence of residual tumors after neoadjuvant chemotherapy. This could ultimately impact surgical management of the patient. Breast MRI evaluation can be incorporated in the management of a patient during treatment as well as after treatment has concluded. It has been reported that MRI can provide evidence of response to therapy 6 weeks after the start of chemotherapy treatment.28 Overall, there is agreement in the literature that ©2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
Breast MRI Indications
FIGURE 2. A–D, A 45-year-old patient presented for MRI evaluation of the extent of disease after a diagnosis of the left breast DCIS measuring 1.2 cm. Mammography examination was negative (A–B); carcinoma was detected on ultrasound (C). Magnetic resonance imaging revealed extensive linear, irregular enhancement in the left breast (D). Magnetic resonance imaging findings altered the patient's management from lumpectomy to mastectomy. At surgical excision, pathology revealed IDC with DCIS measuring 2.8 cm.
MRI is a valuable method for the assessment of tumor response after chemotherapy; however, there are differing opinions regarding the accuracy of MRI at precisely measuring the size of the residual tumor.29 Rieber et al27 found that MRI is helpful in
monitoring response; however, it can be unreliable for determining the size of residual tumor in patients having a significant response to the chemotherapy treatment, finding that MRI often underestimated the amount of residual tumor.28 Other studies have
FIGURE 3. A–B, A 42-year-old unaffected patient presented for breast MRI screening after genetic testing revealed a deleterious mutation in the BRCA1 gene. High-risk MRI detected an enhancing mass in the right breast (A). Targeted ultrasound (B) identified the mass and ultrasound-guided biopsy was performed, resulting in a diagnosis of IDC. ©2014 Lippincott Williams & Wilkins
www.topicsinmri.com
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
331
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
Destounis
FIGURE 4. A–D, Patient presented for MRI evaluation of scar from prior left lumpectomy. Recent mammographic imaging (A–B) demonstrated an area of asymmetry near the scar, which partially resolved on a magnification view (C). Magnetic resonance imaging identified an enhancing mass (D) and MRI biopsy was performed, resulting in a diagnosis of IDC.
FIGURE 5. A–B, A 46-year-old patient presented for MRI evaluation after 7 cycles of chemotherapy treatment. The patient was diagnosed with a 2.3-cm right breast IDC with metastases to lymph nodes (A). On posttreatment MRI (B), previously seen lymphadenopathy was no longer present and the site of IDC was no longer enhanced, with reduction in size to 8 mm. At surgical excision, IDC measured 2.0 cm, with 2 of the 21 lymph nodes positive for metastatic disease, demonstrating that MRI underestimated the size of the residual tumor.
332
www.topicsinmri.com
©2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
Breast MRI Indications
FIGURE 6. A–D, A patient presented for MRI evaluation after presenting for evaluation of right bloody nipple discharge. Mammographic and sonographic images were negative (A–B). An attempt was made at ductography but was unsuccessful because of contrast extravasation. Slides of the discharge were hemoccult positive. Magnetic resonance imaging detected abnormal ductal enhancement from the nipple posteriorly (C–D). Pathology at surgical excision revealed extensive DCIS.
reported high correlation between MRI and histology.29–31 On the basis of the literature, MRI has shown to be accurate in identifying cancers in nonresponders and those with partial response to treatment; however, MRI tends to underestimate the size of tumors that have a good response to treatment.32 Orel33 stated that this is likely related to chemotherapy-induced decrease in tumor vascularization and decreased vascular permeability. It is also thought that the ability of MRI to detect residual tumor may be dependent on the chemotherapeutic agent used; the use of taxane-containing regimens has been associated with underestimation of residual tumor on MRI.34 As stated by Orel,33 the use of breast MRI to evaluate tumor response after chemotherapy is the most accurate imaging method, although it is important to be
mindful of the potential for the tumor to be overestimated or underestimated (Fig. 5).
MRI DETECTION OF OCCULT PRIMARY TUMOR Patients with axillary lymph node metastases consistent with breast origin and patients with distant metastases suggestive of primary breast cancer can be management dilemmas for the breast imager. Occult breast cancer in patients presenting with isolated axillary lymph nodes without a known breast cancer represents up to 1% of operable breast cancer.35–37 Published reports on the use of MRI to evaluate occult primary breast cancer have had similar findings.38,39 A small study conducted by Olson et al37
FIGURE 7. A–B, A 48-year-old patient presented for MRI evaluation of bilateral silicone implants because of suspicion of implant leak. Imaging of the right breast (A–B) revealed that portions of the implant wall folded, suggestive of intracapsular implant rupture. ©2014 Lippincott Williams & Wilkins
www.topicsinmri.com
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
333
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
Destounis
FIGURE 8. A–D, A patient presented for diagnostic evaluation of slight skin puckering of the right breast. Mammogram and ultrasound were equivocal (A–B), with suspicious physical examination findings. Bilateral MRI was performed for evaluation of inconclusive workup and revealed a 3.8-cm area of regional enhancement from the subareolar region posteriorly (C–D). Targeted ultrasound and ultrasound-guided biopsy were performed for a diagnosis of invasive mammary carcinoma.
found that MRI identified a primary breast cancer in 70% of patients included in the study. These patients were women with a biopsy-proven metastatic adenocarcinoma to an axillary lymph node without evidence of primary breast cancer. In addition, Lu et al38 performed a similar study reviewing 35 women with occult breast cancer. The study found that MRI revealed primary breast cancer in 21 of the 35 patients. Small mass lesions and lesions with ductal or segmental enhancement were found to be common features in patients with occult breast cancer and the predominant type of histology was invasive ductal carcinoma (IDC) of moderate grade. The authors also noted that the rate of triplenegative breast cancer may be higher in cases of occult breast cancer. Stomper et al39 performed a small analysis of 8 patients and found that breast MRI can identify the primary tumor site and influence management of patients presenting with clinically and mammographically occult primary breast carcinomas. The use of breast MRI is indicated when evaluating axillary metastases with unknown primary tumor.
EVALUATION OF SUSPICIOUS DISCHARGE It has been reported that the incidence of malignancy in patients presenting with discharge ranges from 5% to 20%.40 There
334
www.topicsinmri.com
is benefit from imaging with mammography, ultrasound, and galactography/ductography. However, there are cases where further evaluation is required (Fig. 6). Traditionally, when clinical evaluation was negative, major duct excision would be the next step for the patient. However, although research on the use of MRI in the evaluation of discharge is somewhat limited, there have been promising findings because the technology has proven its ability to detect otherwise occult breast cancer. A study by Tokuda et al41 evaluated 47 patients with suspicious nipple discharge with MRI and found that MRI was able to provide clinically useful information. Further, Ballesio et al42 found when evaluating 44 patients with discharge and negative mammographic findings that MRI was able to diagnose ductal disease. Similarly, Nakahara et al43 reported that MRI was able to detect all malignancies in the study cohort. Facilities may find that breast MRI is a beneficial option, especially when galactography/ductography is not available.
EVALUATION OF IMPLANT INTEGRITY According to the ACR guidelines, breast MRI may be indicated for evaluating patients with implants.5 The ACS stated that, when performing breast MRI to evaluate silicone implants, a noncontrast MRI can be used, whereas contrast MRI can aid ©2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
in the evaluation of silicone, saline, and/or free injections with silicone, paraffin, or polyacrylamide gel. Findings on MRI representing implant rupture include intracapsular findings (keyhole appearance, subcapsular line, and linguine sign) and extracapsular findings (extracapsular rupture). Studies have shown that MRI is more sensitive for the detection of implant rupture than other imaging methods (Fig. 7). Everson et al44 compared findings of mammography, sonography, computed tomography, and MRI as well as determined that MRI was more sensitive and specific for detecting implant rupture. Similarly, a study by Di Benedetto et al45 found a sensitivity of 93% and a specificity of 73% for MRI compared with 68% and 81% for mammography as well as 77% and 69% for ultrasound, respectively. This study found that mammography and ultrasound were very specific for the detection of extracapsular rupture, whereas overall MRI was the most sensitive for the detection of implant rupture. Breast MRI is an effective imaging method when there is suspicion of an implant rupture.
MRI EVALUATION AFTER INCONCLUSIVE WORKUP Because of the high sensitivity of MRI, the technology can be used to problem solve after equivocal imaging findings with mammography, ultrasound, and physical examination (Fig. 8). It has been suggested that, when there is a negative MRI when evaluating inconclusive workup, the presence of invasive cancer is excluded.46 Although, there are also reports documenting the false-negative rates of MRI from 4% to 12%.47–50 Lee et al50 evaluated the usefulness of MRI for the evaluation of equivocal mammography cases and found that MRI was helpful as an adjunct to evaluate these cases. Magnetic resonance imaging was able to help determine the need for biopsy and, in doing so, was able to diagnose malignancies that might otherwise have been undiagnosed. Further, a negative MRI allowed for surveillance through mammography rather than biopsy. The use of MRI in the setting of equivocal workup with mammography and ultrasound is beneficial, although it is important to not replace the standard imaging workup with MRI. It is important to keep in mind the average specificity of the technology, which does lead to an increased number of false-positive findings and biopsies performed.
MRI-GUIDED BIOPSY Breast MRI performed for any indication can identify suspicious findings that are not detected through mammography, ultrasound, or physical examination. Because of this, a method to biopsy MRI-only lesions is necessary. It is helpful to use targeted ultrasound as the first step after a lesion is identified on MRI. However, targeted ultrasound can fail to identify these MRI-detected lesions in up to 77%,51 although it has also been reported that targeted ultrasound has the ability to identify a correlate in up to 70%.52 In cases where the lesion is not demonstrated on targeted ultrasound, MRI biopsy is indicated. Studies have proven that MRI-guided biopsy is a fast and reliable alternative to surgical excision.53–56 Nonvisualization of lesions at MRI biopsy can occur and has been reported to occur in up to 13%.56 In cases such as these, it is important to perform short-term follow-up to ensure stability. When a facility performs breast MRI, a method to accurately sample MRI-only lesions is vital.
Breast MRI Indications
continue to advance. Breast MRI has proven its benefit in evaluating patients with a recent breast cancer diagnosis as well as patients at high risk for the development of breast cancer. Breast imaging facilities will have to continue to evaluate and reassess the indications following the current guidelines for breast MRI and the evolving needs of the patients.
REFERENCES 1. Holland R, Veling S, Mravunac M, et al. Histologic multifocality of Tis, T1-2 breast carcinomas. Implications for clinical trials of breast-conserving surgery. Cancer. 1985;56:979–990. 2. Anastassiades O, Iakovou E, Stavridou N, et al. Multicentricity in breast cancer. A study of 366 cases. Am J Clin Pathol. 1993;99:238–243. 3. Schwartz G, Patchesfsky A, Feig S, et al. Multicentricity of non-palpable breast cancer. Cancer. 1980;45:2913–2916. 4. Vaidya J, Vyas J, Chinoy R, et al. Multicentricity of breast cancer: whole-organ analysis and clinical implications. Br J Cancer. 1996;74: 820–824. 5. ACR Practice Guideline for the Performance of Contrast-Enhanced Magnetic Resonance Imaging (MRI) of the Breast. http://www.acr.org/ Quality-Saftey/Standards-Guidelines-by-Modality/MRI. Accessed February 18, 2014. 6. Lehman CD, Gatsonis C, Kuhl CK, et al. MRI evaluation of the contralateral breast in women with recently diagnosed breast cancer. N Engl J Med. 2007;356:1295–1303. 7. Fischer U, Kopka L, Grabbe E. Breast carcinoma: effect of preoperative contrast-enhanced MR imaging on the therapeutic approach. Radiology. 1999;213:881–888. 8. Kuhl C, Schmiedel A, Morakkabiti N. Breast MR imaging of the asymptomatic contralateral breast in the work-up or follow-up of patients with unilateral breast cancer. Radiology. 2000;217:268. 9. Lee SG, Orel SG, Woo IJ, et al. MR imaging screening of the contralateral breast in patients with newly diagnosed breast cancer: preliminary results. Radiology. 2003;226:773–778. 10. Liberman L, Morris EA, Kim CM, et al. MR imaging findings in the contralateral breast of women with recently diagnosed breast cancer. AJR Am J Roentgenol. 2003;180:333–341. 11. Kuhl CK, Schrading S, Bieling HB, et al. MRI for diagnosis of pure ductal carcinoma in situ: a prospective observational study. Lancet. 2007;370: 485–492. 12. Allen LR, Lago-Toro CE, Hughes JH, et al. Is there a role for MRI in the preoperative assessment of patients with DCIS? Ann Surg Oncol. 2010;17:2395–2400. 13. Houssami N, Turner R, Macaskill P, et al. An individual person data meta-analysis of preoperative magnetic resonance imaging and breast cancer recurrence. J Clin Oncol. 2014;32:392–401. 14. Saslow D, Boetes C, Burke W, et al. American Cancer Society guidelines for breast screening with MRI as an adjunct to mammography. CA Cancer J Clin. 2007;57:75–89. 15. Kriege M, Brekelmans CT, Boetes C, et al. Efficacy of MRI and mammography for breast-cancer screening in women with a familial or genetic predisposition. N Engl J Med. 2004;351:427–437. 16. Kuhl C, Weigel S, Schrading S, et al. Prospective multicenter cohort study to refine management recommendations for women at elevated familial risk of breast cancer: the EVA trial. J Clin Oncol. 2010;28:1450–1457.
CONCLUSIONS
17. Lehman CD, Blume JD, Weatherall P, et al. Screening women at high risk for breast cancer with mammography and magnetic resonance imaging. Cancer. 2005;103:1898–1905.
The use of breast MRI has evolved for the last decade. As radiologists continue to evaluate the technology, the role will
18. Morris EA, Liberman L, Ballon DJ, et al. MRI of occult breast carcinoma in a high-risk population. AJR Am J Roentgenol. 2003;181:619–626.
©2014 Lippincott Williams & Wilkins
www.topicsinmri.com
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
335
Topics in Magnetic Resonance Imaging • Volume 23, Number 6, December 2014
Destounis
19. Sardanelli F, Podo F, Santoro F, et al. Multicenter surveillance of women at high genetic breast cancer risk using mammography, ultrasonography, and contrast-enhanced magnetic resonance imaging (the high breast cancer risk Italian 1 study): final results. Invest Radiol. 2011;46:94–105. 20. Warner E, Plewes DB, Hill KA, et al. Surveillance of BRCA1 and BRCA2 mutation carriers with magnetic resonance imaging, ultrasound, mammography, and clinical breast examination. JAMA. 2004;292: 1317–1325. 21. Berg WA, Zhang Z, Lehrer D, et al. Detection of breast cancer with addition of annual screening ultrasound or a single screening MRI to mammography in women with elevated breast cancer risk. JAMA. 2012;307:1394–1404. 22. Yilmaz MH, Esen G, Ayarcan Y, et al. The role of US and MR imaging in detecting local chest wall tumor recurrence after mastectomy. Diagn Interv Radiol. 2007;13:13–18. 23. Davis PL, McCarty KS Jr. Sensitivity of enhanced MRI for the detection of breast cancer: new, multicentric, residual, and recurrent. Eur Radiol. 1997;7:S289–S298. 24. Kuhl CK, Schmutzler RK, Leutner CC, et al. Breast MR imaging screening in 192 women proved or suspected to be carriers of a breast cancer susceptibility gene: preliminary results. Radiology. 2000;215:267–279. 25. Warner E, Plewes DB, Shumak RS, et al. Comparison of breast magnetic resonance imaging, mammography, and ultrasound for surveillance of women at high risk for hereditary breast cancer. J Clin Oncol. 2001;19:3521–3531. 26. Stoutjesdijk MJ, Boetes C, Jager GJ, et al. Magnetic resonance imaging and mammography in women with a hereditary risk of breast cancer. J Natl Cancer Inst. 2001;93:1095–1102. 27. Rieber A, Brambs HJ, Gabelmann A, et al. Breast MRI for monitoring response of primary breast cancer to neo-adjuvant chemotherapy. Eur Radiol. 2002;12:1711–1719. 28. Rosen EL, Blackwell KL, Baker JA, et al. Accuracy of MRI in the detection of residual breast cancer after neoadjuvant chemotherapy. AJR Am J Roentgenol. 2003;181:1275–1282. 29. Weatherall PT, Evans GF, Metzger GJ, et al. MRI vs. histologic measurement of breast cancer following chemotherapy: comparison with x-ray mammography and palpation. J Magn Reson Imaging. 2001;13:868–875. 30. Partridge SC, Gibbs JE, Lu Y, et al. Accuracy of MR imaging for revealing residual breast cancer in patients who have undergone neoadjuvant chemotherapy. AJR Am J Roentgenol. 2002;179:1193–1199. 31. Yeh E, Slanetz P, Kopans DB, et al. Prospective comparison of mammography, sonography, and MRI in patients undergoing neoadjuvant chemotherapy for palpable breast cancer. AJR Am J Roentgenol. 2005;184:868–877. 32. Denis F, Desbiez-Bourcier AV, Chapiron C, et al. Contrast enhanced magnetic resonance imaging underestimates residual disease following neoadjuvant docetaxel based chemotherapy for breast cancer. Eur J Surg Oncol. 2004;30:1069–1076. 33. Orel S. Who should have breast magnetic resonance imaging evaluation? J Clin Oncol. 2008;26:703–711. 34. Baron PL, Moore MP, Kinne DW, et al. Occult breast cancer presenting with axillary metastases. Updated management. Arch Surg. 1990;125:210–214. 35. Copeland EM, McBride CM. Axillary metastases from unknown primary sites. Ann Surg. 1973;178:25–27. 36. Rosen PP. Axillary lymph node metastases in patients with occult noninvasive breast carcinoma. Cancer. 1980;46:1298–1306.
336
www.topicsinmri.com
37. Olson JA Jr, Morris EA, Van Zee KJ, et al. Magnetic resonance imaging facilitates breast conservation for occult breast cancer. Ann Surg Oncol. 2000;7:411–415. 38. Lu H, Xu YL, Zhang SP, et al. Breast magnetic resonance imaging in patients with occult breast carcinoma: evaluation on feasibility and correlation with histopathological findings. Chin Med J (Engl). 2011;124: 1790–1795. 39. Stomper PC, Waddell BE, Edge SB, et al. Breast MRI in the evaluation of patients with occult primary breast carcinoma. Breast J. 1999;5:230–234. 40. Tjalma W, Verslegers I. Nipple discharge and the value of MR imaging. Eur J Obstet Gynecol Reprod Biol. 2004;115:234–236. 41. Tokuda Y, Kuriyama K, Nakamoto A, et al. Evaluation of suspicious nipple discharge by magnetic resonance mammography based on breast imaging reporting and data system magnetic resonance imaging descriptors. J Comput Assist Tomogr. 2009;33:58–62. 42. Ballesio L, Maggi C, Savelli S, et al. Role of breast magnetic resonance imaging (MRI) in patients with unilateral nipple discharge: preliminary study. Radiol Med. 2008;113:249–264. 43. Nakahara H, Namba K, Watanabe R, et al. A comparison of MR imaging, galactography and ultrasonography in patients with nipple discharge. Breast Cancer. 2003;10:320–329. 44. Everson LI, Parantainen H, Detlie T, et al. Diagnosis of breast implant rupture: imaging findings and relative efficacies of imaging techniques. AJR Am J Roentgenol. 1994;163:57–60. 45. Di Benedetto G, Cecchini S, Grassetti L, et al. Comparative study of breast implant rupture using mammography, sonography, and magnetic resonance imaging: correlation with surgical findings. Breast J. 2008;14:532–537. 46. Kelcz F, Santyr G. Gadolinium-enhanced breast MRI. Crit Rev Diagn Imaging. 1995;36:287–338. 47. Ghai S, Muradali D, Bukhanov K, et al. Nonenhancing breast malignancies on MRI: sonographic and pathologic correlation. AJR Am J Roentgenol. 2005;185:481–419. 48. Boetes C, Strijk SP, Holland R, et al. False-negative MR imaging of malignant breast tumors. Eur Radiol. 1997;7:1231–1234. 49. Teifke A, Hlawatsch A, Beier T, et al. Undetected malignancies of the breast: dynamic contrast-enhanced MR imaging at 1.0 T. Radiology. 2002; 224:881–888. 50. Lee CH, Smith RC, Levine JA, et al. Clinical usefulness of MR imaging of the breast in the evaluation of the problematic mammogram. AJR Am J Roentgenol. 1999;173:1323–1329. 51. LaTrenta LR, Menell JH, Morris EA, et al. Breast lesions detected with MR imaging: utility and histopathologic importance of identification with US. Radiology. 2003;227:856–861. 52. Destounis S, Arieno A, Somerville PA, et al. Community-based practice experience of unsuspected breast magnetic resonance imaging abnormalities evaluated with second-look sonography. J Ultrasound Med. 2009;28:1337–1346. 53. Liberman L, Morris EA, Dershaw DD, et al. Fast MRI-guided vacuum-assisted breast biopsy: initial experience. AJR Am J Roentgenol. 2003;181:1283–1293. 54. Liberman L, Bracero N, Morris E, et al. MRI-guided 9-gauge vacuum-assisted breast biopsy: initial clinical experience. AJR Am J Roentgenol. 2005;185:183–183. 55. Lehman C, DePeri ER, Peacock S, et al. Clinical experience with MRI-guided vacuum-assisted breast biopsy. AJR Am J Roentgenol. 2005;182:48. 56. Perlet C, Heinig A, Prat X, et al. Multicenter study for the evaluation of a dedicated biopsy device for MR-guided vacuum biopsy of the breast. Eur Radiol. 2002;12:1463–1470.
©2014 Lippincott Williams & Wilkins
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
