Wo m e n ’s I m a g i n g • O r i g i n a l R e s e a r c h Mango et al. MRI of Breast Carcinoma in Augmented Breasts

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Women’s Imaging Original Research

Breast Carcinoma in Augmented Breasts: MRI Findings Victoria L. Mango1 Jennifer Kaplan2 Janice S. Sung2 Chaya S. Moskowitz 3 D. David Dershaw 2 Elizabeth A. Morris 2 Mango VL, Kaplan J, Sung JS, Moskowitz CS, Dershaw DD, Morris EA

Keywords: augmentation, breast carcinoma, implants, MRI DOI:10.2214/AJR.14.13221 Received May 23, 2014; accepted after revision November 20, 2014. Presented at the 2013 ARRS Annual Meeting, Washington, DC. 1 Department of Radiology, Columbia University Medical Center, Herbert Irving Pavilion, 161 Fort Washington Ave, 10th Fl, New York, NY 10032. Address correspondence to V. L. Mango ([email protected]). 2 Department of Radiology, Memorial Sloan-Kettering Cancer Center, Evelyn H. Lauder Breast Center, New York, NY. 3

Memorial Sloan-Kettering Cancer Center, Department of Biostatistics, New York, NY.

This article is available for credit. WEB This is a web exclusive article. AJR 2015; 204:W599–W604 0361–803X/15/2045–W599 © American Roentgen Ray Society

OBJECTIVE. The objective of our study was to characterize the MRI features of breast carcinomas detected in augmented breasts. MATERIALS AND METHODS. A review of the MRI database identified 54 patients with biopsy-proven breast carcinoma in augmented breasts. The images were reviewed for the type and location of the implant and for the characteristics of the carcinoma. The cases included 46 (85%) invasive cancers (invasive ductal carcinoma, n = 35; invasive lobular carcinoma, n = 7; and mixed features, n = 4) and eight (15%) ductal carcinomas in situ. RESULTS. The median age of the patients at diagnosis was 49 years (range, 28–72 years). Thirty-eight of the 54 cancers (70%) were palpable. The mean tumor size was 2.8 cm (range, 0.6–9.6 cm). Of the 54 cancers, 34 (63%) presented as masses and 20 (37%) as nonmass enhancement on MRI. There was no detectable difference between implant position and lesion morphology (p = 0.55) or tumor size (p = 1.00). Twenty of 54 (37%) carcinomas abutted the implant, 13 (24%) abutted the pectoralis major muscle, and two (4%) invaded the pectoralis major muscle. Of the tumors abutting the implant, 18 of 20 (90%) spread along the implant capsule for more than 0.5 cm. This pattern of tumor spread was more common in breasts with retroglandular implants (9/16, 56%) than in those with retropectoral implants (9/38, 24%) (p = 0.03). MRI detected the index carcinoma in 16 of 54 (30%) cases, showed a greater extent of disease than was visible on mammography or ultrasound in 21 of 52 (40%) cases, and detected an unsuspected contralateral carcinoma in three of 54 (6%) cases. CONCLUSION. In augmented breasts, breast cancer often contacts either the implant or the pectoralis major muscle. Tumor spread along the implant contour is more often seen with retroglandular implants than with retropectoral implants. MRI should be considered to assess disease extent in women with augmented breasts before surgery.

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reast augmentation with implants is an increasingly common surgical procedure; 286,274 cases were reported in the United States in 2012, a 35% increase since 2000 [1]. These 2012 cases do not include the additional 72,012 cases of breast reconstruction using implants [1]. In total, more than 2 million women have undergone augmentation mammoplasty in the United States [2], and 69% of these patients were 39 years old or younger at the time of surgery [1]. Although there is no direct association between implants and an increased breast cancer risk [3], as patients with augmented breasts age, the number of breast cancer cases among women with augmented breasts is anticipated to increase [2, 4]. Mammographic screening of women with augmented breasts may be limited because breast implants obscure a significant per-

centage of breast parenchyma on routine views [5] and because implant-displaced views have been reported to allow only a moderate improvement in visualization [6– 8]. Although decreased sensitivity of screening mammography in women with implants has been shown [9], there are conflicting results as to whether the presence of implants delays breast cancer diagnosis [4, 9–11]. Early reports suggested that women with breast implants present at a more advanced stage and have a higher percentage of invasive lesions and metastatic axillary lymph nodes [8, 12]; however, later studies did not confirm those findings [9]. Given the limitations of mammography and the possibility of more extensive disease at presentation, dynamic contrast-enhanced breast MRI may play an important role in imaging breast carcinoma in women with implants [13, 14].

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Mango et al. The appearance of breast carcinoma in patients with augmentation has been described on mammography and ultrasound [7, 15–17]. Although MRI is the imaging modality of choice for the evaluation of implant integrity [18–21], there is little information regarding the role of MRI in the diagnosis and evaluation of breast cancer in women with augmentation [22]. Small case series have been published characterizing the MRI features of breast carcinoma in patients with breast augmentation by silicone or paraffin injection [20, 23, 24]. However, to our knowledge, there are no published data about the MRI appearance of breast carcinoma in patients with implant augmentation. Our study characterizes the MRI features of breast carcinomas detected in breasts augmented with implants, including the relationship of the carcinoma to the implant and to the pectoralis major muscle, and evaluates the utility of MRI in determining the extent of disease in the preoperative setting. Materials and Methods Patient Population An institutional review board–approved HIPAAcompliant retrospective review of the MRI database identified 54 patients with biopsy-proven breast carcinoma in augmented breasts visualized on MRI between 2000 and 2010. The median patient age was 49 years (range, 28–72 years). The implant types included 31 (57%) saline implants, 22 (41%) silicone implants, and one (2%) dual-lumen implant (inner silicone and outer saline). The location of the implants was retropectoral in 38 (70%) and retroglandular in 16 (30%). The implants had been in place a mean of 10 years (range, 0.3–35 years) before breast cancer diagnosis. Thirty-eight of the 54 (70%) cancers were palpable.

Breast MRI was performed for the evaluation of a known carcinoma in 38 (70%) patients, highrisk screening in seven (13%) patients, and problem solving in nine (17%) patients (e.g., axillary metastases with an unknown primary and a palpable finding with negative mammography and ultrasound findings). Eight of 54 (15%) patients had a personal history of breast carcinoma. Four patients had undergone ipsilateral mastectomy and implant reconstruction, and a subsequent recurrence was visualized on MRI. The remaining four patients with a personal history of cancer had a history of a contralateral breast carcinoma (one patient) or an ipsilateral carcinoma treated with lumpectomy (three patients).

Breast MRI Technique MRI examinations were performed with the patient prone on a 1.5- or 3-T commercially available system using a dedicated surface breast coil. Standard breast MRI sequences included a localizing sequence followed by a sagittal non–fat-suppressed T1-weighted sequence and a sagittal fat-suppressed T2-weighted sequence. A T1-weighted 3D fat-suppressed fast spoiled gradient-echo sequence was then performed before and three times after a rapid bolus injection of gadopentetate dimeglumine (Magnevist, Bayer HealthCare) administered IV (0.1 mmol/L per kilogram of body weight). After contrast injection and saline bolus injection, images were obtained in a sagittal projection. Additionally, an axial contrastenhanced T1-weighted sequence was performed. The section thickness was 0.3 cm with no gap, and a minimum matrix of 256 × 256 was used. After the examination, the unenhanced images were subtracted from the contrast-enhanced images on a pixel-by-pixel basis to produce three contrast-enhanced subtraction sequences. Maximumintensity-projection images were created using the first contrast-enhanced sequence and the first contrast-enhanced subtracted data.

TABLE 1: Imaging Features of Breast Carcinomas in Augmented Breasts ­Visualized on MRI Retroglandular Implants (n = 16)

Retropectoral Implants (n = 38)

Total (n = 54)

Mass

9

25

34 (63)

Nonmass

7

13

20 (37)

Imaging Features Enhancement type, no. (%) of tumors

0

0

0 (0)

Mean size of tumor (cm)

Focus

2.4

3.0

2.8

Cancer contacts implanta, no. (%) of tumors

10

10

20 (37)

Parallels implant contour for > 0.5 cm, no. (%) of tumors

9

9

18 (33)

aCancer contacting the implant is based on MRI appearance of abnormal enhancement at the site of known

carcinoma inseparable from the implant. In retropectoral implants, tumor appeared to contact the implant where it was not covered by the pectoralis major muscle or where the muscle was too thin to be visualized using MRI.

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Image Interpretation The breast MRI examinations were interpreted on a PACS by one fellowship-trained breast radiologist with 10 years’ experience reading breast MRI. The reader was not blinded to carcinoma location, patient history, or prior examinations and was provided all available sequences for interpretation. Images were reviewed for fibroglandular density, background enhancement, implant type, and implant location. The index cancer was identified, and the following features of the index cancer were recorded: location in the breast, size, enhancement type (focus, mass, nonmass), shape, margins, internal enhancement pattern, distribution, signal intensity on T2-weighted imaging, qualitative kinetic pattern, and relationship to the implant and pectoralis major muscle. Other findings were recorded, such as additional lesions in either breast, nipple retraction, skin involvement, and lymphadenopathy. If additional breast lesions were identified, only the MRI features of the index carcinoma were reviewed. The relevant information from the electronic medical record was obtained including patient age, clinical presentation, date of augmentation, and tumor and node pathology. Mammography and ultrasound findings, if available, were noted in each patient and were correlated with the MRI findings.

Data Collection and Analysis The Fisher exact test was used for comparisons involving categoric data. The Wilcoxon rank sum test was used to compare continuous distributions. A value of p < 0.05 was considered statistically significant.

Results Breast MRI Findings: Index Carcinoma The cancers had a mean size of 2.8 cm (range, 0.6–9.6 cm) and were most commonly located in the upper outer quadrant (28/54, 52%). The pathologic diagnoses were eight (15%) ductal carcinomas in situ and 46 (85%) invasive cancers (35 invasive ductal carcinomas, seven invasive lobular carcinomas, and four tumors with mixed features). Mass enhancement was seen in 34 of 54 (63%) cases and nonmass enhancement in 20 (37%) cases (Table 1). Carcinoma was not described as a focus (< 0.5 cm) in any case. Of the 34 tumors with mass enhancement, the shape was irregular in 30 (88%) and oval in four (12%) and the margins were noncircumscribed in 34 (100%). Enhancement was heterogeneous in 22 (65%) and rim in 12 (35%). Of the 20 tumors with nonmass enhancement, distribution was segmental in six (30%), regional in five (25%), linear in five

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MRI of Breast Carcinoma in Augmented Breasts (25%), focal in two (10%), linear branching in one (5%), and diffuse in one (5%). Nonmass internal enhancement was clumped in 16 of 20 (80%) and heterogeneous in four of 20 (20%). The kinetic pattern was available for 53 tumors and was assessed qualitatively: 31 tumors (58%) showed washout; 20 (38%), plateau; and two (4%), persistent. Of the 54 cancers, 20 (37%) abutted the implant on MRI. Eighteen of 20 (90%) spread along the implant capsule for more than 0.5 cm. Tumor spread along the implant capsule was more common in women with retroglandular implants (9/16, 56%) than in those with retropectoral implants (9/38, 24%) (p = 0.03) (Table 1). In 10 of 20 (50%) cases, cancer spread along the implant extended for more than 1.0 cm. In retropectoral implants, the tumor appeared to contact the implant where it was not covered by the pectoralis major muscle or where the muscle was too thin to be visualized on MRI. Thirteen of 54 (24%) carcinomas abutted the pectoralis major muscle, and eight of 13 (62%) paralleled the muscle contour for more than 0.5 cm. Two of 54 (4%) tumors invaded the pectoralis major muscle; in these two cases, one case with a retroglandular implant (1/16, 6%) and the other with a retropectoral implant (1/38, 3%), abnormal muscle enhancement was visualized on MRI and invasion was confirmed by final pathology. There was no detectable difference between implant position and lesion morphology (p = 0.55) or tumor size (p = 1.00). There was also no association between

A

TABLE 2: Added Value of MRI in 54 Patients With Breast Carcinoma in ­Augmented Breasts Added Value of MRI by MR Findings Depicted Index cancer not seen on mammography or ultrasound Tumor size larger compared with size on mammography or ultrasound Multifocal disease not seen on mammography or ultrasound MRI showed multicentric disease not seen on mammography or ultrasound Occult contralateral carcinoma

No. (%) of Women 16 (30) 5 (9) 4 (7) 12 (22) 3 (6)

MRI led to biopsy of additional findings (excluding index tumors)a

12 (22)

aBiopsy results were benign disease in seven patients and malignant disease in five patients.

Breast MRI Findings: Lymphadenopathy Suspicious adenopathy was identified on MRI in eight of 54 (15%) patients; however, pathology results were positive in 18 of 48 (38%) patients. There was no statistically significant association between implant composition and nodal disease (p = 0.26) or between the number of years an implant had been in place and positive nodal disease at pathology (p = 0.23).

made in these cases. The index carcinoma was visualized mammographically in 31 of 50 cases (62%), but the mammographic findings were considered vague in four of those cases. The remaining 19 cancers (38%) were mammographically occult. Ultrasound studies were available for review and correlation with MRI findings in 42 of 54 (78%) patients. Of the 42 patients with available ultrasound correlation, ultrasound showed the index cancer in 28 (67%). An additional seven cancers were visualized using targeted ultrasound after MRI. Seven of 42 cancers (17%) were sonographically occult.

Breast MRI Findings: Correlation With Mammography and Ultrasound Fifty of the 54 (93%) patients had undergone mammography within 6 months of carcinoma diagnosis, and correlation of mammography findings with MRI findings was

Breast MRI: Added Value MRI identified the index carcinoma in 16 of 54 (30%) cases not previously identified on mammography or ultrasound (Table 2). MRI showed the tumor to be larger compared with the size on mammography or ul-

B

C

the number of years an implant had been in place and tumor size (p = 0.78) or invasive pathology (p = 0.60).

Fig. 1—Ductal carcinoma in situ (DCIS) extending along implant in 44-year-old woman with family history of breast carcinoma and retroglandular saline implants for 10 years. A–C, Sagittal fat-suppressed contrast-enhanced subtraction (A), sagittal fat-suppressed contrast-enhanced non-subtracted (B), and sagittal subtraction maximumintensity-projection (C) MR images of right breast show 3.4-cm nonmass enhancement (arrows) at 12-o’clock position extending along implant in segmental distribution. Ultrasound-guided core biopsy yielded DCIS.

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Mango et al.

A

B

C

Fig. 2—Tumor abutting retropectoral implant in 52-year-old woman with saline implants for 6 years. A, Sagittal contrast-enhanced subtraction MR image of left breast obtained to determine extent of disease for known invasive ductal carcinoma at 7-o’clock, a 1.0-cm irregular mass (white arrow) with an adjacent focus. B and C, Sagittal contrast-enhanced subtraction (B) and sagittal subtraction maximum-intensity-projection (C) MR images demonstrate additional rim-enhancing mass (black arrows) at 9-o’clock abutting implant 4 cm from known carcinoma (white arrow). This finding was site of additional disease at pathology.

trasound in five cases. MRI identified additional disease not detected on mammography or ultrasound: MRI showed that disease was multifocal in four of 54 (7%) patients and multicentric in 12 of 54 (22%) patients. An occult contralateral carcinoma was found in three of 54 (6%) patients. Excluding the index carcinomas, MRI findings led to 12 additional biopsies, seven (58%) of which yielded benign disease and five (42%), malignant. Discussion This study shows the range of MRI features of carcinoma in augmented breasts. The majority of tumors, 63%, showed mass enhancement mostly with an irregular shape and noncircumscribed margins. Of the tumors that appeared with nonmass enhancement, distribution was variable—most commonly, segmental (Fig. 1) followed by regional and linear. Focal enhancement, linear branching enhancement, and diffuse enhancement were seen less commonly. Most nonmass internal enhancement was clumped. All three kinetic patterns were visualized; the most common kinetic pattern was a washout pattern, which was seen in 58% of cases. There was no detectable difference between implant position and lesion morphology (p = 0.55) or tumor size (p = 1.00). MRI provides a unique opportunity to evaluate the relationship of breast carcinoma to the implant and pectoralis major mus-

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cle, whose position can be altered by implant placement. Preoperative knowledge of cancer spread along the implant capsule or pectoralis major muscle may affect surgical planning. Additionally, radiologists’ awareness of this pattern of tumor growth aids in accurate identification of the full extent of disease on MRI, which may affect patient treatment decisions. Further study is necessary to determine the full impact of this knowledge on treatment and prognosis. Cancer often abuts the implant on MRI, as seen in 20 of 54 (37%) cases with tumor spreading along the implant contour for more than 0.5 cm in 90% (18/20) and extending more than 1.0 cm in 50% (10/20) (Fig. 1). Abnormal enhancement paralleling the implant contour for more than 0.5 cm occurred more often with retroglandular implants (9/16, 56%) than with retropectoral implants (9/38, 24%) (p = 0.03). In retropectoral implants, tumor appeared to contact the implant where it was not covered by pectoralis major muscle or where the muscle was stretched too thin to be visualized using MRI (Fig. 2). Surgical disruption of tissue planes from prior augmentation probably allows tumor to spread along the implant and pectoralis major muscle. The pectoralis major muscle abutted tumor in 13 of 54 (24%) cases with carcinoma paralleling the muscle contour in eight of those cases (Fig. 3). Although abnormal enhancement contacted the pectoralis major muscle in 13 cases,

only two cases showed abnormal muscle enhancement suspicious for invasion and had final pathology results confirming muscle invasion: one case with a retroglandular implant (1/16, 6%) and the other with a retropectoral implant (1/38, 3%). Thus, the pectoralis major muscle is still at risk for invasion regardless of implant location. Our study population underwent MRI at the discretion of their ordering clinician and therefore is a selected sample of women with augmented breasts with breast carcinoma. However, we found that MRI may be a valuable adjunct to mammography and ultrasound given that the index carcinoma was initially identified with MRI in 16 of 54 (30%) patients and was not seen on a previous mammography or ultrasound study. Breast MRI also appears to be valuable in evaluating for multifocal and multicentric disease in addition to detecting occult contralateral carcinoma in this patient population. Further study is necessary to determine what role MRI should play in patients with breast implants. Identification of nodal disease with MRI was limited. Suspicious adenopathy was identified on MRI in eight of 54 (15%) patients; however, pathology was positive in 18 of 48 (38%) patients. It is interesting that our pathology results are comparable to previously published studies of patients with augmentation and breast carcinoma, which showed nodal metastases at pathology in 36–47%

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MRI of Breast Carcinoma in Augmented Breasts

A

B

C

Fig. 3—Carcinoma parallels pectoralis major muscle in 45-year-old woman with retropectoral saline implants for 5 years. MRI was performed to determine extent of disease after ultrasound-guided core biopsy of 0.7-cm mass yielded invasive ductal carcinoma (IDC). A, Sagittal non–fat-saturated T1-weighted MR image shows retropectoral implant. B and C, Sagittal contrast-enhanced subtraction (B) and sagittal subtraction maximum-intensity-projection (C) MR images show 5.0-cm clumped mass enhancement (arrows) contacting and paralleling contour of pectoralis major muscle consistent with IDC. No abnormal muscle enhancement was identified on MRI, and pathology confirmed no pectoralis major muscle invasion.

of cases [7, 8, 12, 15, 16]. These results are much higher than the 18% lymph node positivity reported in the general population with screening-detected cancers on digital mammography [25]. In our patient population, 85% (46/54) of women had invasive carcinoma, which is also comparable to previously published results that showed 73–91% invasive carcinomas in women with breast carcinoma and augmentation [7–9, 12, 15, 16]. A large percentage—70% (38/54)—of the cancers in our study were palpable. It is possible that clinicians were more inclined to select patients for MRI in the setting of a palpable finding, which may have potentially influenced our results. However, this observation is supported by previous studies showing patients with implants and breast cancer are likely to present with clinical symptoms [7–9, 12, 15, 16]. Patients who had prior ipsilateral mastectomy with implant reconstruction would be expected to have recurrence suspected on the basis of clinical symptoms given that these patients do not undergo routine screening. This was true in our study. In a previous report, Miglioretti et al. [9] reported that women with augmentation who had undergone mammography within 1 year of a cancer diagnosis were more likely than women without augmentation to present with symptoms, 47% versus 35%, respectively. Additional studies of women with im-

plants and breast carcinoma have shown that 55–97% present with a palpable concern [7, 8, 12, 15, 16]. It has been suggested that palpating breast masses may be easier in this patient population because of the lower volume of native breast, which is splayed by the implant [4], and because implants provide a firm platform against which to palpate a tumor [26]. There is also anterior displacement and compression of tissue by the implant [27]. It has also been suggested that women with augmentation may be more “breast aware” or body conscious and therefore are more likely to present with clinical symptoms [4, 9]. Palpability may also partially be attributed to the average tumor size of 2.8 cm in our patient population. This average tumor size is comparable to an average tumor size of 2.6 cm in augmented breasts reported in a previous study by Skinner et al. [4]; in that study, Skinner et al. found that the average tumor size in augmented breasts was not statistically different than that in nonaugmented breasts. The limitations of our study include the small number of patients and its retrospective nature. Given that our patient population was selected for MRI at the discretion of ordering clinicians, caution about making generalizations to all women with implants and breast carcinoma is appropriate. Also, eight of 54 (15%) patients had a personal history of breast carcinoma, which could further contribute to

selection bias. The MRI examinations were performed over a 10-year period, so MR image quality and MRI techniques differed, which possibly influenced the results. In conclusion, in augmented breasts the expected pattern of breast cancer can be altered by contact with and growth around the implant or the pectoralis major muscle. Tumor spread along the implant contour is seen more often with retroglandular implants than with retropectoral implants. The pectoralis major muscle is vulnerable to invasion regardless of implant location. MRI may be a valuable adjunct to mammography and ultrasound in evaluating for multifocal and multicentric disease in addition to detecting occult contralateral carcinoma in this patient population but is limited in identifying nodal disease. Our data suggest that MRI should be considered to assess disease extent before surgery for women with all types of implants given the limitations of mammography and ultrasound. References 1. American Society of Plastic Surgeons website. 2012 Plastic surgery statistics report. www.plasticsurgery. org/news/plastic-surgery-statistics/2012-plasticsurgery-statistics.html. Accessed November 23, 2013 2. McCarthy CM, Pusic AL, Disa JJ, et al. Breast cancer in the previously augmented breast. Plast Reconstr Surg 2007; 119:49–58 3. Hoshaw SJ, Klein PJ, Clark BD, et al. Breast im-

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