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10.1245/s10434-006-9195-5
Annals of Surgical Oncology 14:1051-1057 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Results of MRI Screening for Breast Cancer in High-Risk Patients with LCIS and Atypical Hyperplasia

Elisa Rush Port1, Anna Park1, Patrick I. Borgen3, Elizabeth Morris2 and Leslie L. Montgomery1

1 Breast Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, USA
2 Department of Radiology, Memorial Sloan-Kettering Cancer Center, New York, USA
3 Maimonides Cancer Center, New York, USA

Correspondence: Address correspondence and reprint requests to: Elisa Rush Port; MRI-1026, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10021, USA; E-mail: porte{at}mskcc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 CONCLUSIONS
 REFERENCES
 
Background: Magnetic resonance imaging (MRI) can detect breast cancer in high-risk patients, but is associated with a significant false-positive rate resulting in unnecessary breast biopsies. More data are needed to define the role of MRI screening for specific high-risk groups. We describe our experience with MRI screening in patients with atypical hyperplasia (AH) and lobular carcinoma in situ (LCIS).

Methods: We retrospectively reviewed data from our high-risk screening program prospective database for the period from April 1999 (when screening MRI was first performed at our institution) to July 2005. Patients with AH or LCIS demonstrated on previous surgical biopsy were identified. All patients underwent yearly mammography and twice yearly clinical breast examination. Additional screening MRI was performed at the discretion of the physician and patient.

Results: We identified 378 patients; 126 had AH and 252 had LCIS. Of these, 182 (48%) underwent one or more screening MRIs (mean, 2.6 MRIs; range, 1–8) during this period, whereas 196 (52%) did not. Those who had MRIs were younger (P < 0.001) with stronger family histories of breast cancer (P = 0.02). In MRI-screened patients, 55 biopsies were recommended in 46/182 (25%) patients, with 46/55 (84%) biopsies based on MRI findings alone. Cancer was detected in 6/46 (13%) MRI-generated biopsies. None of the six cancers detected on MRI were seen on recent mammogram. All six cancers were detected in five patients (one with bilateral breast cancer) with LCIS; none were detected by MRI in the AH group. Thus, cancer was detected in 5/135 (4%) of patients with LCIS undergoing MRI. The yield of MRI screening overall was cancer detection in 6/46 (13%) biopsies, 5/182 (3%) MRI-screened patients and 5/478 (1%) total MRIs done. In two additional MRI-screened patients, cancer was detected by a palpable mass in one, and on prophylactic surgery in the other and missed by all recent imaging studies. For 196 non-MRI-screened patients, 21 (11%) underwent 22 biopsies during the same period. Eight of 22 (36%) biopsies yielded cancer in seven patients. All MRI-detected cancers were stage 0–I, whereas all non-MRI cancers were stage I–II.

Conclusion: Patients with AH and LCIS selected to undergo MRI screening were younger with stronger family histories of breast cancer. MRI screening generated more biopsies for a large proportion of patients, and facilitated detection of cancer in only a small highly selected group of patients with LCIS.

Key Words: Magnetic resonance imaging • Atypical hyperplasia • Lobular carcinoma in situ • Breast cancer screening


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 CONCLUSIONS
 REFERENCES
 
Breast cancer is the most common solid malignancy in the United States with an estimated 214,640 new cases in 2006.1 However, not all women are at equal risk for breast malignancy development; a wide variety of factors increase risk, including genetic predisposition,2 family history,3 pathology findings on a previous biopsy,4,5 a history of previous mantle radiation3,6 and other factors related to reproductive history.3 For many women with the aforementioned risk factors, absolute or relative risk of breast cancer development can be quantified. When appropriate based on level of risk, preventive strategies such as the use of tamoxifen,7 or increased surveillance, which may not be appropriate for the general population, may be implemented.

Screening magnetic resonance imaging (MRI) can detect breast cancer that is otherwise occult. However, screening MRI can be associated with false-positive findings requiring unnecessary biopsies and follow-up examinations that are extensive, stressful and costly.8–11 Because of this, appropriate patient selection for additional screening with MRI is of paramount importance. Currently, the only definitive guidelines regarding patient selection for MRI screening come from the National Comprehensive Cancer Network, which indicates that MRI screening should be considered in patients with a strong family history or known BRCA mutation; MRI is not mentioned in screening guidelines outlined for other high-risk populations.12 While the role of screening MRI in high-risk populations has been studied, most studies involve heterogeneous populations of patients with a wide variety of risk factors.8,13–19 Furthermore, many studies have focused specifically on MRI screening in the BRCA-heterozygote population. Thus, results from these screening studies may be skewed by disproportionate representation of an exceptionally high-risk population.9,13 More detailed data regarding the yield of MRI screening in specific high-risk groups are needed so that MRI can be added to screening regimens judiciously.

Women who have undergone a breast biopsy that demonstrates either atypical ductal hyperplasia (ADH) or atypical lobular hyperplasia (ALH) have been shown to have a 20% absolute lifetime risk of breast cancer development when compared with the average woman’s risk of approximately 10%.4 Similarly, women found to have lobular carcinoma in situ (LCIS) on excisional biopsy have a reported risk of approximately 25% of breast cancer development.5 No study to date has focused specifically on screening MRI in patients deemed to be at increased risk for breast cancer based on the findings of ADH/ALH or LCIS on previous biopsy. Here, we describe our experience of screening MRI in this population of patients.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 CONCLUSIONS
 REFERENCES
 
Patient Selection
We retrospectively reviewed the Memorial Sloan-Kettering Cancer Center (MSKCC) high-risk breast cancer surveillance program prospective database to identify patients who had undergone MRI screening between April 1999 (when MRI screening was first performed at MSKCC) and July 2005. Patients who had undergone a previous surgical biopsy demonstrating LCIS or ADH/ALH were identified. Patients with known or suspected BRCA mutations were not included in this group and represented a separate population in our surveillance program; however, those with a concomitant family history of breast cancer were included in this analysis.

For all patients who underwent biopsies at outside institutions, pathology was reviewed by a dedicated breast pathologist at Memorial MSKCC. The surveillance regimen for patients in this group includes biannual clinical breast examination and yearly screening mammography. In general, screening, ultrasound was not part of routine care for this patient population. Targeted sonography was implemented to further evaluate findings on physical examination, mammography, or MRI.

Two staff breast surgeons (Elisa Port and Leslie Montgomery) were responsible for the care of patients with atypical hyperplasia (AH) and LCIS in the MSKCC high-risk screening program. Both surgeons discussed additional screening MRI with all new patients with no co-morbid conditions that would preclude their ability to undergo MRI screening and potential associated procedures. Screening MRI was ultimately performed at the discretion of the physician and patient. Reasons for patients not participating in MRI screening included claustrophobia, prior gadolinium allergy, fear of false-positive results and insurance- and reimbursement-related concerns. When possible, to facilitate reimbursement, documentation regarding risk status and the appropriateness of MRI screening was provided by the physician. All MRI screening examinations were performed at MSKCC, as were all follow-up imaging studies, biopsies, and subsequent surgery.

All P values were calculated using the Student t-test; Fisher’s exact test was used for all categorical variables; and statistical software programs used were SPSS 12.0, SPSS Inc. (Chicago, IL, USA) and StatX-act 5 (Cytel Software Corp, Cambridge, MA, USA).

Breast MRI Technique
MRI examinations were performed with the patient prone in a 1.5-T commercially available system (Sigma, General Electric Medical Systems, Milwaukee, WI, USA) using a dedicated surface breast coil.20 Our imaging sequence includes a localizing sequence followed by a sagittal fat-suppressed T2-weighted sequence (TR/TE, 4000/85). A T1-weighted three-dimensional, fat-suppressed fast spoiled gradient-echo sequence (17/2.4; flip angle, 35°; bandwidth, 31.25 Hz) was then performed one time before and three times after a rapid bolus injection of 0.1 mmol/L of gadopentetate dimeglumine (Magnevist, Berlex, Wayne, NJ, USA) per kilogram of body weight, delivered through an intravenous catheter.

Image acquisition starts after contrast material injection and saline bolus. Images were obtained sagittally for an acquisition time per volumetric acquisition of less than 3 min each. Total imaging time per breast, including three contrast-enhanced acquisitions, is approximately 20 min. Section thickness is 2–3 mm with no gap using a matrix of 256 by 192 and a field of view of 18–22 cm. Frequency is in the anteroposterior direction. After the examination, the unenhanced images are subtracted from the first contrast-enhanced images on a pixel-by-pixel basis.

Breast MRI Interpretation
Breast MRI examinations are interpreted according to previously described criteria.21 In our study, breast imaging specialists interpreted MRIs in conjunction with clinical history and the results of other breast imaging studies, including mammograms and sonograms, if performed. Level of suspicion was reported on a scale of 0–5: 0 indicated need for additional imaging; 1, no abnormal enhancement; 2, benign enhancement; 3, probably benign, short-term follow-up recommended (specified as either at different times in the patient’s menstrual cycle or in 6 months); 4, suspicious; and 5, highly suggestive of malignancy.

MRI-detected lesions referred for biopsy primarily included masses with spiculated or irregular margins, irregular shape, heterogeneous or rim enhancement and nonmass lesions that showed linear or segmental enhancement. Interpreting radiologists referred other lesions for biopsy in conjunction with clinical history and other imaging studies. Tiny (1-mm) foci of enhancement or diffuse-stippled enhancement generally do not prompt biopsy. Classification is based primarily on lesion morphology; however, kinetic features are visually assessed on the three contrast-enhanced image acquisitions with quantitative kinetic curves generated in specific cases at the request of the interpreting radiologist.

For nonpalpable, mammographically occult, MRI-detected lesions warranting biopsy, correlative sonography was recommended at the discretion of the radiologist interpreting the MRI examination if it is thought that the lesion might be sonographically evident and amenable to sonographically guided biopsy. If the lesion is not seen on sonography, MRI-guided needle localization for surgical excision or MRI-guided vacuum-assisted biopsy was performed using previously described methods.20


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
CONCLUSIONS
 REFERENCES
 
Three hundred and seventy-eight patients, 126 with ADH/ALH and 252 with LCIS, were identified as participants in the surveillance program. Of these, 182 (48%) underwent screening MRI (mean 2.6 MRIs, range 1–8) during this period, whereas 196 (52%) did not. Of the 126 patients with atypia, 47 (37%) underwent screening MRI, while 79 (63%) did not. For patients with LCIS, 135 (54%) underwent MRI, while 117(46%) did not. Those who had MRIs were significantly younger, more likely to be premenopausal, and had a stronger family history of breast cancer (Table 1Go). Only those who were asymptomatic and in whom MRI had been performed strictly for screening purposes were included. The frequency of MRI screening over the study period varied: 60/182 patients underwent only one MRI during the entire study period, 39 patients underwent two MRIs, 30 patients underwent three, 27 patients underwent four, 16 patients underwent five, nine patients underwent six and one patient underwent eight MRI examinations. Thus, a total of 478 screening MRIs were performed. For patients in the MRI-screened group, 55 biopsies were recommended in 46/182 (25%) patients over the duration of the study period, beginning from the time each individual patient initiated MRI screening. Of these 55 biopsies, 46 biopsies in 39/182 (21%) patients were generated by MRI findings alone. Cancer was detected in 6/ 46(13%) biopsies indicated for MRI findings alone. One patient had bilateral biopsies yielding cancer and thus the six cancers were found in 5/182 patients (3%) who underwent MRI screening, and in 5/478 (1%) of all MRIs performed. In four of five patients with MRI-detected cancer, cancer was detected on the first MRI exam. In the fifth patient, cancer was detected on the third MRI. Patients with MRI-detected cancer who did not undergo mastectomy continued to have MRI screening.


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  		TABLE 1. Patient characteristics
 
The nine additional biopsies were performed based on findings on physical examination or mammography. All of these nine patients had had a normal MRI examination within the prior 6 months. Eight of these biopsies based on non-MRI findings were benign, while one patient developed an interval palpable mass that proved to be a cancer approximately 6 months after a normal MRI and mammogram. In addition, one patient in the MRI screening group ultimately underwent bilateral risk-reducing mastectomy, which demonstrated a cancer on pathology with a recent normal MRI. Thus, a total of eight cancers were detected in the MRI screening group, six of which were detected by MRI alone. The sensitivity of MRI was 75%, specificity was 92%, and the positive predictive value was 13% in this group.

All five patients with MRI-detected cancers, as well as the patient found to have cancer incidentally at surgery were patients with an initial diagnosis of LCIS, while the patient who developed the interval cancer had atypia. Thus, the yield of MRI screening was 5/135 (4%) patients with LCIS. In contrast, MRI was not helpful in identifying otherwise occult cancer in any of the 47 patients with atypia.

For the 196 patients who did not undergo MRI screening, 22 biopsies were performed in 21/196 (11%) total patients with either LCIS or atypia based on physical examination or mammogram findings. Cancer was found in 8/22 (36%) biopsies in seven patients (one with bilateral). A significantly larger number of patients who underwent MRI screening required biopsy compared with the non-MRI-screened group (46/182 vs. 21/196; P = 0.0002)

While the numbers of cancers diagnosed in both the MRI- and non-MRI-screened groups were small, there was a trend toward earlier diagnosis for MRI-detected cancers, with MRI-detected cancers being stage 0 or I compared with stages I and II for those who developed cancer and did not undergo MRI screening (Table 3Go). In addition, four of four invasive cancers detected by MRI were smaller than 1 cm. In contrast, only 4/8 primary invasive cancers were smaller than 1 cm in the non-MRI group.


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  		TABLE 3. Stage of cancers detected
 
Of the 182 patients in the MRI-screened group, 87 (48%) patients, had at least one MRI interpreted as BIRADS 3, requiring short-term follow-up MRI for further evaluation; 136 of 478 (28%) total MRIs performed were interpreted as BIRADS-3. A total of 127 of 182 (70%) patients who underwent MRI screening had at least one BIRADS 3, 4 or 5 MRI result over their course of MRI screening, thus requiring either biopsy or short-term follow-up MRI.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 CONCLUSIONS
REFERENCES
 
Only two options have been proven effective for cancer prevention in patients at increased risk for breast cancer; neither of these options have been widely implemented: risk-reducing mastectomy involves extensive surgery;22 tamoxifen, the only FDA-approved chemopreventive agent, is associated with rare but serious side effects, the fear of which frequently deter women from taking it.7,23 Given recently published results of the Study of Tamoxifen and Raloxifene (STAR) trial24 and previous results reported in the Multiple Outcomes of Raloxifene Evaluation MORE trial,25 raloxifene, a second chemopreventive agent will almost certainly soon be approved for breast cancer prevention. Early reports indicate that raloxifene is associated with a similar side-effect profile as tamoxifen. Thus, it is unclear whether or not raloxifene will achieve more widespread patient acceptance for breast cancer prevention purposes. Given the limited primary preventive options, secondary prevention (intensified surveillance with the goal of early detection) plays a central role in the care of women at increased risk for breast cancer.

Early detection of breast cancer through mammographic screening has translated to survival benefit.26 Yet, approximately 10% of all newly diagnosed breast cancers are mammographically occult.27 MRI has been shown to detect mammographically occult breast cancer in a variety of different clinical scenarios. In those with an occult primary, MRI can identify the primary lesion in approximately 70% of the cases, thereby facilitating breast conservation therapy.28 In patients with a known breast cancer, MRI screening of the contralateral breast demonstrates an otherwise occult cancer in approximately 4%.15

Screening studies of patients at increased risk for breast cancer with MRI have demonstrated the MRI detection of an otherwise occult cancer in 1–7% of the patients.8,9,11 In these studies, the eligibility criteria for MRI screening vary considerably. Most studies of high-risk populations have focused on women with suspected or proven BRCA mutations. Given this group’s exceptionally high risk of developing breast cancer, the yield of cancer detection by MRI in this group may not represent cancer detection rates of MRI screening for all high-risk patients. For example, Kuhl et al.29 demonstrated that 43 cancers were detected in a total of 1,701 MRI examinations in women at increased risk based on genetic predisposition, some of whom had a personal history of previous breast cancer. Of these 43 cancers, 19 were detected by MRI alone. In this group, cancer was detected at a higher rate in known mutation carriers (7% prevalence rate; 5% incidence rate over ensuing years) compared with patients without a known mutation but nevertheless deemed to be at increased lifetime risk of 20–40% (2.5% prevalence rate; 2.7% incidence rate for ensuing years).

Leach et al.11 studied a similar group of patients aged 35–49 years with either known BRCA or P53 mutations or high-risk status based on strong family history. MRI sensitivity in cancer detection was superior to that of mammography and markedly so for BRCA1 mutation carriers. These findings led to the conclusion that MRI may play a significant role in breast cancer screening for this group at highest risk.

In the largest study of MRI screening in women at increased risk from the Netherlands, Kriege et al.9 screened 1,909 eligible women including 358 BRCA-heterozygotes and the rest with family histories constituting a 15% or greater risk. While MRI was more sensitive than mammography, the specificity and positive-predictive value of MRI was lower, generating more unnecessary biopsies.

The MRI screening study that represents the most heterogeneous population at increased risk comes from MSKCC,8 and includes those with a prior breast cancer, genetic predisposition, those with atypia and/or LCIS and those who had undergone prior mantle radiation. Of this group of 367 patients, 43 (12%) patients had undergone a previous biopsy demonstrating atypia or LCIS as their main risk factor. In this group, biopsy was recommended in 10 of 43 (23%) patients, demonstrating cancer in 1 of 43 (2%).

The variation in yield of cancer detection based on degree of risk coupled with the high false-positive rate emphasizes the importance of data that provide insight regarding actual benefit for specific high-risk populations. To our knowledge, this is the first study focusing on the results of MRI screening in patients with the specific risk factor of AH or LCIS. Information regarding risks and benefits of MRI screening in this specific population is important for physician and patient decision-making regarding the pursuit of MRI screening based on a patient’s risk factors.

While patients screened with MRI were theoretically a higher risk group than those who did not given their stronger family histories, the cancer detection rate was the same in both groups. Our data demonstrated no added value of MRI screening for improved cancer detection among the population of patients with AH (albeit a small population), and a small benefit for women with LCIS (4% rate of cancer detection). In addition, patients who underwent MRI screening required a significantly greater number of biopsies to pursue MRI findings, and the majority of women who underwent MRI screening required short-term follow-up examination or biopsy at some point. These data emphasize the importance of discussion with the patient prior to embarking on an MRI screening regimen to prepare her for the possible need for biopsy and/or short-term follow-up examinations.

There are conflicting data regarding whether or not separate risk factors, such as the combination of ADH and family history, are additive to increase overall patient risk for breast cancer. When calculating estimated risk of breast cancer using the widely implemented Gail model,3 family history combined with atypical hyperplasia portends a higher overall risk than that for a patient with atypia alone, and thus for the individual with these two separate risk factors, the overall effect is additive. With the scenario of additive risk, one could anticipate an increased initiative for MRI screening in patients with a family history combined with LCIS or AH. Other recent studies suggest that given a history of AH, the addition of a family history of breast cancer did not significantly further increase the overall risk.30

In our population, patients with a family history of breast cancer and either LCIS or atypia were significantly more likely to undergo MRI screening. While the number of patients in our study who ultimately developed cancer was small, the addition of family history did not have any effect on the yield of MRI screening with regard to cancer detection. Of the five patients who developed cancer detected by MRI, only one reported any family history.

As demonstrated in previously mentioned studies, interval cancers presenting as a palpable mass despite recent negative imaging studies including MRI underscore the importance of frequent clinical follow-up and surveillance in patients at increased risk.

Results from this study are limited, because they represent an experience in a highly selected and self-selected patient population. Nevertheless, it provides some data that may be helpful in discussions and decision-making in a specific population of patients at increased risk for breast cancer for which MRI screening is being considered.


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  		TABLE 2. Profiles of patients who developed cancer
 
Received for publication March 23, 2006. Accepted for publication July 13, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 CONCLUSIONS
 REFERENCES
 

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