Pure Ductal Carcinoma in Situ: A Range of MRI Features

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1 Women s Imaging Pictorial Essay Raza et al. MRI of Ductal arcinoma in Situ Women s Imaging Pictorial Essay Downloaded from by on 1/9/18 from IP address opyright RRS. For personal use only; all rights reserved Sughra Raza 1 Monica Vallejo Sona. hikarmane Robyn L. irdwell Raza S, Vallejo M, hikarmane S, irdwell RL 1 ll authors: Department of Radiology, righam and Women s Hospital, 75 Francis St., oston, M ddress correspondence to S. Raza (sraza1@partners.org). ME This article is available for ME credit. See for more information. JR 28; 191: WOMEN S IMGING Keywords: breast, ductal carcinoma in situ, MRI, pure ductal carcinoma in situ, women s imaging DOI:1.2214/JR Received February 5, 28; accepted after revision March 18, X/8/ merican Roentgen Ray Society Pure Ductal arcinoma in Situ: Range of MRI Features OJETIVE. The purpose of this article is to describe and illustrate the variety of common morphologic features, enhancement patterns, and kinetics of pure ductal carcinoma in situ (DIS) on dynamic contrast-enhanced MRI of the breast, using the merican ollege of Radiology I-RDS lexicon. ONLUSION. reast MRI plays an important role in the detection of DIS, which most often appears as nonmass clumped enhancement, in a ductal or segmental distribution, with variable enhancement kinetics. D uctal carcinoma in situ (DIS) or intraductal carcinoma is a noninvasive malignancy characterized by the clonal proliferation of malignant epithelial cells originating in the terminal ductal lobular unit, with no histologic evidence of invasion of the basement membrane. It is most often asymptomatic and may involve multiple sites separated by normal tissue in the same ductal system or in different ductal systems. Typically, part of the natural pathophysiology of DIS is calcification in the affected ducts. These calcifications are visible in up to 9% of DIS cases diagnosed on mammography alone [1], most commonly in clustered, linear, or segmental distributions. pproximately 1 2% of DIS may present as a mass or other parenchymal lesion such as architectural distortion with or without calcifications [2]. With the widespread use of mammographic screening, DIS now accounts for 2 3% of breast cancers detected at screening mammography [3], and evidence suggests that approximately 14 75% of cases may progress to invasive carcinoma [4]. When intraductal carcinoma is treated with surgery achieving negative margins and no radiation therapy, the recurrence rate is 22.5% [4]. The recurrence rate is higher if close or positive margins are present at the time of surgery. Regardless of treatment method (mastectomy, lumpectomy with radiation therapy, or wide surgical excision alone), half the recur- rences are invasive ( 2% with distant metastases at 1 years) [5]. Whole-breast radiation therapy reduces the recurrence rate by 5%, and treatment of estrogen receptor positive cases with tamoxifen reduces this risk by another 5% [4]. Therefore, early detection and accurate assessment of the extent of disease are important for thorough breastconserving treatment and to achieve the best possible prognosis. ecause calcifications are not present in all cases of DIS, such lesions are mammographically occult, contributing to a mammographic sensitivity of 7 8% [3]. Similarly, because all involved areas may not calcify equally, the extent of disease is often underestimated on mammography. Therefore, alternative means of detecting DIS have been explored, including the use of contrastenhanced MRI. reast MRI has emerged as an important tool in the detection and characterization of breast cancer, showing sensitivity ranging from 9 1% for invasive carcinoma [6, 7]. In contrast, the reported sensitivity of MRI for detection of DIS is lower, ranging from 77% to 96% [8], perhaps because of differences in tumor size, degree of angiogenesis and histology, and differences in imaging protocols [9]. Despite these limitations, the distinct advantage of MRI in the detection of carcinoma is that, based on tumor vascularity, vessel density, and permeability, even noncalcified mammographically occult areas of DIS can be seen because of abnormal contrast uptake. JR:191, September

2 Raza et al. Downloaded from by on 1/9/18 from IP address opyright RRS. For personal use only; all rights reserved Imaging Technique During the study period, May 24 to December 27, breast MRI examinations were performed at our facility with the patient prone in either a Signa 1.5-T or HDX 3-T commercially available system (both from GE Healthcare) using a dedicated breast surface coil. Our routine protocol included a threeplane localizing sequence followed by a sagittal fat-suppressed T2-weighted sequence and axial fast spoiled gradient-recalled echo T1- weighted non fat-saturated sequences for each breast before the administration of contrast material. Dynamic sagittal VIRNT (volume imaging for breast assessment) T1- weighted fat-suppressed 3D fast spoiled gradient-recalled echo (3D FSPGR) sequences were then performed before and four times after the IV administration of 2 ml of contrast material (Magnevist [gadopentetate dimeglumine], ayer Healthcare) at 2 ml/s. The first contrast-enhanced dynamic sequence was obtained at approximately 2 minutes, followed by three more consecutive sequences. Finally, an axial T1-weighted fat-suppressed 3D FSPGR delayed sequence was performed. Postprocessed subtracted images, maximumintensity-projection (MIP) images, and ngiogenesis Maps (Dstream, version 4.1, onfirma) were processed by a computeraided evaluation system (Dstream). MRI haracteristics of DIS Enhancement Patterns The I-RDS lexicon [1] describes three types of enhancing lesions seen on breast MRI: first, focus, defined as a spot of enhancement that is too small (< 5 mm) to allow further morphologic characterization; second, mass, or a 3D space-occupying lesions, usually round, oval, or irregular in shape; and third, nonmasslike enhancement, which is enhancement of an area that is not a mass and is characterized by distribution and internal enhancement patterns. Previous studies [11, 12] have shown that pure DIS most often presents as nonmasslike enhancement (Figs. 1 11) and less commonly as a mass (Fig. 12). Nonmasslike Enhancement Distribution Patterns I-RDS descriptors demonstrate variability in their use as well as their specificity and positive predictive value for DIS. Furthermore, the older literature was hampered by the lack of an existing lexicon, leading to great variability in the frequency of reported distributions. Since 23, when the first edition of the I-RDS MRI lexicon was published, some authors have chosen to group linear, ductal, and segmental distributions [13, 14], whereas others distinguish segmental from ductal and linear [11, 12]. Segmental distribution is defined as a triangular area of enhancement, apex pointing to the nipple, suggesting a duct or its branches (Figs. 5, 7, and 1). The I-RDS lexicon defines linear as a line that may not conform to a duct (Fig. 3) and ductal as a line that may have branching, conforming to a duct (Figs. 1, 2, and 4). Less common distributions seen in pure DIS are regional, enhancement in a large volume of tissue not conforming to a ductal distribution, geographic [1] (Figs. 8, 9, and 11); and focal area, enhancement in a confined area, less than 25% of quadrant [1] (Fig. 6). Internal Enhancement Patterns The most common internal enhancement pattern found in pure DIS is clumped, cobblestone like enhancement, with occasional confluent areas [11, 12] (Figs. 1 3, 5 7, and 11). Other enhancement patterns include heterogeneous or nonuniform enhancement in a random pattern (Figs. 8 and 9). Kinetic Patterns The kinetic curve shape is created by perfusion and diffusion of contrast material from the blood vessels to the extracellular space. Reports suggest that perfusion rates increase as a lesion progresses from in situ to invasive [15], and that microvessel density plays a role as well [16, 17]. With current MRI techniques, as outlined earlier, a temporal resolution of 12 seconds will not image lesion perfusion but rather capture the diffusion of the contrast material [11]. On the basis of the I-RDS lexicon [1], the initial phase of enhancement, within 2 minutes or when the shape of the kinetic curve starts to change, is described as fast, medium, or slow. The delayed phase (after 2 minutes or after the curve starts to change) is described as either persistent (type I), continued increase in signal over time; plateau (type II), signal intensity does not change over time after initial rise; or washout (type III), signal intensity decreases from the highest point after an initial rise [1] (Fig. 13). The pharmacokinetic time signal intensity curves associated with pure DIS are variable. In the initial phase, rapid uptake is most commonly seen; in the delayed phase, persistent, plateau, and washout kinetics are all seen [11] (Fig. 13). recent article [11] observed no significant difference in the morphology or kinetic enhancement characteristics among the different nuclear grades of pure DIS. Recognizing that breast MRI is evolving, both technically and with regard to the lexicon, the degree to which morphologic and kinetic characteristics play a role in interpretation and recommendations varies between masses and nonmasslike enhancing lesions. ecause as many as 3% of DIS cases seen as nonmasslike enhancement show the least worrisome pattern of persistent enhancement, interpretation and final recommendations should be based on morphology rather than on the kinetic curves [18, 19]. In addition, DIS is not usually visible on either non-fat-suppressed or fat-suppressed T2-weighted sequences or unenhanced T1- weighted images because it either mimics normal breast parenchyma or, less likely, appears relatively hypointense [2]. onclusion ontrast-enhanced dynamic MRI of the breast is complementary to mammography in the detection of DIS because enhancement may be seen in areas of calcified as well as noncalcified intraductal carcinoma. This allows detection of noncalcified disease and more accurate assessment of the extent of disease, improving treatment and prognosis. On MRI, DIS can manifest in a range of appearances, frequently as clumped nonmasslike enhancement, in a ductal or segmental distribution, most commonly showing rapid initial contrast uptake with plateau, persistent, or washout kinetics in the delayed phase. References 1. Dershaw DD, bramson, Kinne DW. Ductal carcinoma in situ: mammographic findings and clinical implications. Radiology 1989; 17: Farshid G, Downey P, Gill PG. typical presentations of screen-detected DIS: implications for pre-operative assessment and surgical intervention. reast 27; 16: Ernster VL, allard-arbash R, arlow WE, et al. Detection of ductal carcinoma in situ in women undergoing screening mammography. J Natl ancer Inst 22; 94: Leonard GD, Swain SM. Ductal carcinoma in situ: complexities and challenges. J Natl ancer Inst 24; 96: ijker N, Peterse JL, Duchateau L, et al. Risk factors for recurrence and metastasis after breast- 69 JR:191, September 28

3 MRI of Ductal arcinoma in Situ conserving therapy for ductal carcinoma-in-situ: Schmidt R, Karczmar GS. Pure ductal carcino- 25; 14: analysis of European Organization for Research ma in situ: kinetic and morphologic MR charac- 16. Guidi J, Fischer L, Harris JR, Schnitt SJ. Mi- and Treatment of ancer Trial J lin On- teristics compared with mammographic appear- crovessel density and distribution in ductal carci- col 21; 19: ance and nuclear grade. Radiology 27; 245: noma in situ of the breast. J Natl ancer Inst 6. Orel SG, Schnall MD. MR imaging of the breast ; 86: for the detection, diagnosis, and staging of breast 12. Rosen EL, Smith-Foley S, DeMartini W, Eby 17. Heffelfinger S, Miller M, Yassin R, Gear R. Downloaded from by on 1/9/18 from IP address opyright RRS. For personal use only; all rights reserved cancer. Radiology 21; 22: Morris E. Review of breast MRI: indications and limitations. In: Miller W, ed. Seminars in roentgenology. Philadelphia, P: Saunders, 21: Morris E, Liberman L. Ductal carcinoma in situ. In: Morris E, Liberman L, eds. reast MRI: diagnosis and intervention. Philadelphia, P: Springer, 24: Orel SG, Mendonca MH, Reynolds, Schnall MD, Solin LJ, Sullivan D. MR imaging of ductal carcinoma in situ. Radiology 1997; 22: Ikeda D, Hylton M, Kuhl, et al. reast Im aging Reporting and Data System, I-RDS: Magnetic Resonance Imaging (I-RDS:MRI) Reston, V: merican ollege of Radiology, Jansen S, Newstead GM, be H, Shimauchi, PR, Peacock S, Lehman D. I-RDS MRI enhancement characteristics of ductal carcinoma in situ. reast J 27; 13: Menell JH, Morris E, Dershaw DD, bramson F, rogi E, Liberman L. Determination of the presence and extent of pure ductal carcinoma in situ by mammography and magnetic resonance imaging. reast J 25; 11: Morakkabati-Spitz N, Leutner, Schild H, Traeber F, Kuhl. Diagnostic usefulness of segmental and linear enhancement in dynamic breast MRI. Eur Radiol 25; 15: Furman-Haran E, Schechtman E, Kelcz F, Kirshenbaum K, Degani H. Magnetic resonance imaging reveals functional diversity of the vasculature in benign and malignant breast lesions. ancer ngiogenic growth factors in preinvasive breast disease. lin ancer Res 1999; 5: Kriege M, rekelmans T, oetes, et al. Efficacy of MRI and mammography for breast-cancer screening in women with a familial or genetic predisposition. N Engl J Med 24; 351: Kuhl. MR imaging for surveillance of women at high familial risk for breast cancer. In: Kuhl, ed. Magnetic resonance imaging clinics: breast MR imaging. Philadelphia, P: Saunders, 26: Kvistad K, Rydland J, Vainio J, et al. reast lesions: evaluation with dynamic contrast-enhanced T1-weighted MR imaging and with T2*-weighted first-pass perfusion MR imaging. Radiology 2; 216: Fig. 1 7-year-old woman with recent (< 6 months previously) diagnosis of atypical lobular hyperplasia by stereotactic biopsy of right breast calcifications. ilateral MRI was performed to rule out occult malignancy. In this and all subsequent figures, sagittal image is from first run of dynamic contrast-enhanced series, and axial image is from delayed contrast-enhanced series. and, Sagittal () and axial () T1-weighted fat-suppressed 3D fast spoiled gradient-recalled echo images after contrast injection show 1.5-cm area of ductal and clumped enhancement (arrows) in contralateral breast, with persistent enhancement kinetics and no mammographic correlate. MRI-directed core biopsy followed by excision revealed ductal carcinoma in situ, cribriform and solid types, intermediate nuclear grade, with central necrosis. JR:191, September

4 Raza et al. Downloaded from by on 1/9/18 from IP address opyright RRS. For personal use only; all rights reserved D Fig year-old woman with recently diagnosed right breast cancer underwent bilateral MRI to evaluate extent of disease. and, Sagittal () and axial () T1-weighted fatsuppressed 3D fast spoiled gradient-recalled echo dynamic images show known cancer (arrows) in right breast. and D, In contralateral lower, outer breast, area of ductal clumped enhancement (arrows) with washout kinetics is seen. No sonographic or mammographic correlates were found. MRI-guided core biopsy followed by surgical excision reveals ductal carcinoma in situ (DIS) solid, cribriform, and micropapillary types, intermediate grade with central necrosis. E and F, Pathology images (E, low magnification; F, high magnification) of estrogen receptor and progesterone receptor positive, HER2/neu-negative DIS show involved ducts in linear array and little periductal fibrosis (arrows). E F 692 JR:191, September 28

5 MRI of Ductal arcinoma in Situ Downloaded from by on 1/9/18 from IP address opyright RRS. For personal use only; all rights reserved Fig year-old woman with history of low- to intermediate-grade ductal carcinoma in situ (DIS) in left breast who was treated with lumpectomy and radiation therapy 6 years previously. Routine mammogram (not shown) revealed equivocal increase in 5-mm area of calcifications in treated left upper breast. and, Sagittal () and axial () bilateral MR images show area of linear clumped persistent enhancement in left upper outer quadrant (arrows) that did not definitely correlate with mammographic calcifications. MRI-guided core needle biopsy revealed DIS, cribriform and solid types, intermediate nuclear grade, associated microcalcifications, and necrosis. Surgical excision found DIS only. Fig year-old woman with recent diagnosis of invasive ductal carcinoma (thin arrow, ) of left breast. and, Sagittal () and axial () MR images obtained to determine extent of disease shows additional area of rapid ductal homogeneous enhancement (thick arrows) and washout kinetics in upper outer quadrant 3 cm posterior to primary mass (thin arrow, ). Pathology (not shown) revealed ductal carcinoma in situ, cribriform type, high nuclear grade, without necrosis. JR:191, September

6 Raza et al. Downloaded from by on 1/9/18 from IP address opyright RRS. For personal use only; all rights reserved Fig year-old woman with strong family history of breast cancer who presented with palpable right upper outer quadrant lump that was seen on sonography as a 1-cm solid mass. iopsy revealed invasive ductal carcinoma. and, Sagittal () and axial () bilateral MR images obtained to evaluate extent of disease show rapidly enhancing mass (arrows) in axillary tail that corresponds to known cancer. and D, In addition, sagittal () and axial (D) images show cm area of clumped persistent enhancement in segmental distribution in right lower central breast (arrows) without mammographic or sonographic correlates. MRI-directed core biopsy followed by surgical excision revealed extensive ductal carcinoma in situ, solid, cribriform, and clinging types, intermediate grade, with central necrosis. D 694 JR:191, September 28

7 MRI of Ductal arcinoma in Situ Downloaded from by on 1/9/18 from IP address opyright RRS. For personal use only; all rights reserved Fig year-old woman with R1 gene mutation and history of breast-conserving therapy, including radiation therapy, for solid and cribriform intermediate-grade ductal carcinoma in situ (DIS) without necrosis in upper outer right breast 1 year previously. and, ontrast-enhanced T1-weighted fat-suppressed 3D fast spoiled gradient-recalled echo sagittal () and axial () images from routine surveillance MRI show focal area of clumped enhancement (arrows) with plateau kinetics in lower inner contralateral left breast. MRI-directed biopsy revealed DIS, solid and cribriform types, intermediate grade, with necrosis. Fig year-old woman with family history (sister) of breast cancer and recent negative mammogram. and, Sagittal () and axial () screening MR images obtained for surveillance show area of nonmass segmental clumped enhancement (arrows) with plateau kinetics in upper inner left breast. Pathology revealed ductal carcinoma in situ, solid and comedo types, high nuclear grade, with central necrosis. JR:191, September

8 Raza et al. Downloaded from by on 1/9/18 from IP address opyright RRS. For personal use only; all rights reserved Fig year-old woman with palpable right upper outer quadrant nodularity and negative mammography and sonography. and, Sagittal () and axial () MR images show nonmass regional heterogeneous persistent enhancement (arrows) in right lower outer quadrant, and no abnormality in upper breast. MRI-guided core biopsy and subsequent mastectomy (neither shown) revealed extensive ductal carcinoma in situ (DIS) in region of MRI enhancement. DIS was of solid, cribriform, and clinging types, high nuclear grade, without necrosis. Fig. 9 5-year-old woman with strong family history of breast and ovarian cancer (maternal aunts, grandmother, and great aunts). Mammography (not shown) showed group of faint heterogeneous calcifications at 12-o clock position in right breast. and, Sagittal () and axial () MR images show cm nonmass with regional rapid contrast uptake (arrows) in right upper inner quadrant, heterogeneous internal enhancement, and persistent kinetics separate from area of calcifications. Pathology of MRI-directed excision (not shown) revealed ductal carcinoma in situ, cribriform and papillary types, intermediate grade. Surgical biopsy (not shown) of mammographically detected calcifications in superior central breast revealed lobular carcinoma in situ. 696 JR:191, September 28

9 MRI of Ductal arcinoma in Situ Downloaded from by on 1/9/18 from IP address opyright RRS. For personal use only; all rights reserved D E Fig year-old woman who presented with palpable firmness in outer upper quadrant of her left breast while breast-feeding. ilateral mammogram (not shown) showed suspicious pleomorphic calcifications in corresponding region. Stereotactically guided core biopsy (not shown) revealed cribriform and solid types of ductal carcinoma in situ, intermediate nuclear grade., Sagittal MR images obtained to evaluate extent of disease show segmental area of rapid homogeneous enhancement and washout kinetics (arrows) encompassing most of upper outer quadrant. D and E, Extent of involvement is well visualized on 3D maximum intensity projections (arrows). Fig year-old woman with history of grade 2 invasive, mixed ductal and lobular carcinoma in left breast and associated ductal carcinoma in situ (DIS) 2 years previously. Patient was treated with lumpectomy and radiation therapy. On routine follow-up mammography (not shown), new.8-cm right upper outer quadrant mass was seen., Sagittal () and axial ( and ) MR images identify this mammographically detected lesion as rim-enhancing round mass (thick arrow, ) with irregular margins and heterogeneous internal enhancement. In addition, MR images show.5.7 cm nonmass ductal clumped enhancement (thin arrow) with persistent kinetics 4 cm anterior and inferior to mass. Sonographically guided core biopsy of mass (not shown) revealed invasive ductal carcinoma, but area of clumped enhancement was visible only on MRI. Subsequent MRI-guided core biopsy and surgical excision (neither shown) of this nonmass enhancement revealed DIS, solid type, intermediate to high nuclear grade. JR:191, September

10 Raza et al. Downloaded from by on 1/9/18 from IP address opyright RRS. For personal use only; all rights reserved Fig year-old woman with strong family history (mother) of breast cancer. Developing density on screening mammography with no sonographic correlate led to bilateral breast MRI. and, ontrast-enhanced sagittal () and axial () images show 2-cm irregular mass (arrows) with rapid homogeneous enhancement and plateau kinetics in inferior central right breast. Pathology (not shown) revealed ductal carcinoma in situ (DIS), comedo and cribriform types, high nuclear grade, with central necrosis. and D, Pathology images (, low magnification; D, high magnification) show estrogen receptor and progesterone receptor positive, HER2/neu-positive DIS with marked periductal fibrosis (arrows) in contrast to adipose tissue in upper right corner of both images. Involved ducts are clustered, markedly distended, and enlarged. D 698 JR:191, September 28

11 MRI of Ductal arcinoma in Situ Downloaded from by on 1/9/18 from IP address opyright RRS. For personal use only; all rights reserved % hange Time (s) % hange Time (s) Time (s) Fig. 13 Kinetic curve characteristics of pure ductal carcinoma in situ. Graphs were drawn by Dstream computer-aided evaluation system (Dstream, version 4.1, onfirma)., Typical dynamic time intensity curves show initial rapid uptake followed by either persistent increase in signal intensity (type I), associated with 6% risk of malignancy (); signal intensity not increasing after initial rise, reaching plateau (type II), 64% probability of malignancy (); or rapid washout in delayed phase (type III), 87% probability of malignancy () [1]. FOR YOUR INFORMTION This article is available for ME credit. See for more information. % hange JR:191, September